Dr. Sridutt B S October 2016 Department of Neurosurgery...

IMPACT OF TEMPORAL LOBE RESECTION ON APPRECIATION OF MUSIC

AND FACIAL EMOTIONS

Submitted for MCh Neurosurgery

Sree Chitra Tirunal Institute for Medical Sciences & Technology

Thiruvananthapuram


AND FACIAL EMOTIONS – A PROSPECTIVE NON-RANDOMISED

OBSERVATIONAL STUDY

Submitted for MCh Neurosurgery

By

Dr. Sridutt B S

October 2016

Department of Neurosurgery

Tirunal Institute for Medical Sciences & Technology

Thiruvananthapuram – 695011


RANDOMISED

Tirunal Institute for Medical Sciences & Technology


AND FACIAL EMOTIONS

Submitted by :

Programme :

Month & Year of submission :


AND FACIAL EMOTIONS – A PROSPECTIVE NON-RANDOMISED

OBSERVATIONAL STUDY

Dr. Sridutt B S

MCh Neurosurgery

October 2016


RANDOMISED

MCh Neurosurgery

CERTIFICATE

This is to certify that the thesis entitled “Impact of temporal lobe resection on

appreciation of music and facial emotions – a prospective non-randomised

observational study” is a bonafide work of Dr. Sridutt B S and was conducted in the

Department of Neurosurgery, Sree Chitra Tirunal Institute for Medical Sciences and Technology,

Thiruvananthpuram, under my guidance and supervision.

Prof. Suresh Nair N

Head of Department,

Department of Neurosurgery,

SCTIMST,

Thiruvananthapuram

DECLARATION

The thesis entitled “Impact of temporal lobe resection on appreciation of music and

facial emotions – a prospective non-randomised observational study” is a consolidated

report based on a bonafide study of the period from July 2015 to September 2016, done by me

under the Department of Neurosurgery, Sree Chitra Tirunal Institute for Medical Sciences and

Technology, Thiruvananthpuram.

This thesis is submitted to SCTIMST in partial fulfillment of the rules and regulations for MCh

Neurosurgery examination.

Dr. Sridutt B S

Department of Neurosurgery,

SCTIMST,

Thiruvananthpuram

ACKNOWLEDGEMENT

This project work is the end result of the combined efforts of not just me, but a lot of people

working along with me and with the invaluable guidance of my teachers. I take this opportunity

to express my gratitude in all humility to them.

First up, I would express my humble gratitude to God almighty for giving me the

opportunity to study and practice medicine and help humanity in whatever little way I

presumably can.

Prof. Suresh Nair N, Head of Department, Neurosurgery, SCTIMST, besides being a great

surgeon, is a wonderful human being. His guidance, valuable inputs, expert supervision and

untiring help throughout the period of this study has made it possible for this work to take its

present form. Without his knowledge and foresight it would have been impossible to complete

this project in time. His uncompromising work ethics admixed with his remarkable sense of

humor has kept us on our toes throughout and helped us steer through times of darkness and

gloom. I take great pride in addressing myself as his student. His teachings would light the long

and tedious road that lies ahead towards success.

Prof. Mathew Abraham, Professor, Neurosurgery, has been my principal guide for this

project. He is a versatile surgeon and a treasure house of resourcefulness. Without his expertise

in this field, it would have been next to impossible for me to recruit subjects for this project and

evaluate them. He has stood by me at each and every step of this project. His constant

encouragement and guidance was quintessential for completion of this study.

I am highly indebted to Dr. George C Vilanilam, Associate Professor, Neurosurgery, for

providing all the resources and every possible help and encouragement needed for completion

of this project. His constant reminders and deadlines were invaluable for the progress of

this work. I am thankful to him for all his untiring efforts.

I take this opportunity to express my deep sense of gratitude and regards for my teachers Prof.

Girish Menon, Dr. Easwer H V, Dr. Krishnakumar K, Dr. Jayanand Sudhir B and Dr.

Prakash Nair for their kind help, consistent encouragement and healthy suggestions.. Their vast

knowledge, acute perception and critical analysis aided me in innumerable ways. Their cooperation

and assistance was indispensible.

I express my sincere gratitude to Mrs. Renu Joji, for her invaluable support in conducting the

neuro-psychological test in this study.

I also express my gratitude to my friends and colleagues Dr. Ranjit Rangnekar,

Dr. Vihang Sali and Dr. Vishal Thakur who have always been there at times of need and ever

ready to lend a helping hand. I express my sincere gratitude to Dr. Bimal Sahoo,

Dr. Gopikrishnan, Dr. Pankaj Shivhare, Dr. Shashank, Dr. Gograj Garhwal, Dr. Nithin Raj,

Dr. Palak Jaiswal and Dr. Pradeepanand Vaidya who have provided me with invaluable

assistance whenever required.

I take this opportunity to express my gratitude and indebtedness to my parents who have been a

pillar of support throughout my career and have imbibed in me the values and principles which

have kept me in good stead. I also thank my wife and other family members for being a constant

source of support and encouragement.

October 2016 Sridutt B S

TABLE OF CONTENTS

1. INTRODUCTION .............................................................................................. 1

2. REVIEW OF LITERATURE ........................................................................... 3

2.1 ANATOMY OF TEMPORAL LOBE ............................................................ 3

2.2 PHYSIOLOGY OF TEMPORAL LOBE ....................................................... 8

2.3 NEURO-COGNITIVE IMPLICATIONS OF ATL ..................................... 14

3. AIMS & OBJECTIVES .................................................................................. 26

4. MATERIALS & METHODS ......................................................................... 27

5. OBSERVATIONS & RESULTS .................................................................... 35

6. DISCUSSION ................................................................................................... 69

7. CONCLUSION ................................................................................................. 82

8. REFERENCES ................................................................................................. 83

9. ANNEXURES ................................................................................................... 88

9.1 MASTER CHART ....................................................................................... 88

9.2 KEY TO MASTER CHART ....................................................................... 91

9.3 IEC APPROVAL LETTER ......................................................................... 92

9.4 ORIGINALITY REPORT ........................................................................... 94

9.5 CONSENT FORMS ..................................................................................... 95

9.6 CASE PROFORMA .................................................................................... 97

1

1. INTRODUCTION:

Surgery is frequently considered as the treatment of choice for patients with

medically refractory temporal lobe epilepsy. Anterior temporal lobectomy (ATL)

along with resection of mesial temporal structures i.e. with amygdalo-

hippocampectomy is the most commonly performed epilepsy surgery worldwide.

ATL is generally considered a safe surgery with long term clinically significant

neuro-cognitive sequelae occurring in only a small fraction of patients undergoing

ATL. Nevertheless, ATL is not completely devoid of neuro-cognitive risk. Several

studies have reported both short term and long term neuro-cognitive changes

associated with ATL. These changes may at times be serious enough to necessitate

interventions and rehabilitative measures to reduce the morbidity of patients in

performing activities of daily living.

Most studies in literature that measure outcome after epilepsy surgery, the quality

of life profile and neuro-cognitive outcome are usually measured at 6 months to

one year post surgery. Following up these patients for longer intervals has

frequently shown that the neuro-cognitive functions for most patients will

gradually improve over time and ultimately attain levels that are almost

comparable to pre-operative values.

2

However, there is no clear consensus regarding the best time interval for evaluating

neuro-cognitive function after epilepsy surgery to detect any early impairments

that may exist so that such patients may be expeditiously directed toward the

appropriate cognitive rehabilitation therapy. The data on early cognitive

impairments in such patients needs to be evaluated to address their needs in terms

of cognitive rehabilitation and other interventions.

Therefore, the aim of our study is to compare and contrast the pre-operative

neuropsychological profile in patients undergoing ATL for epilepsy with

immediate postoperative and early post-operative (at 3 months) performance. We

hypothesized that short-term evaluation beginning at six weeks after resective

epilepsy surgery would reveal early changes in neuro-cognitive function that may

help to identify patients who may need expeditious referral to rehabilitation, which

may ultimately influence decisions such as early return to work or school.

3

2. REVIEW OF LITERATURE:

2.1 ANATOMY OF THE TEMPORAL LOBE:

The temporal lobe is one of the five lobes of the cerebrum. The temporal lobe lies

inferior to the sylvian fissure, which separates it from the frontal and parietal lobes.

The temporal lobe is limited posteriorly by an imaginary line joining the pre-

occipital incisure to the parieto-occipital sulcus.

For descriptive purposes, the temporal lobe is studied with reference to 3 surfaces

– the lateral surface, the medial surface and the inferior surface.

Lateral surface - Lateral surface is divided into three parallel gyri by two sulci.

The superior and inferior temporal sulci divide the lateral surface into superior,

middle and inferior temporal gyri. These gyri terminate anteriorly at the temporal

pole. Along its superior margin, the superior temporal gyrus is continuous with the

gyri on the floor of the posterior ramus of the sylvian fissure. These gyri vary in

number and they extend anterolaterally around the insula as transverse temporal

gyri of Heschl. Gyri of Heschl and adjoining area of superior temporal gyrus forms

the primary auditory cortex (Area 42).

The middle temporal gyrus lies between the superior and inferior temporal sulci.

The temporal horn and the ambient and the crural cisterns are located deep to the

middle temporal gyrus. The inferior temporal gyrus lies below the inferior

4

temporal sulcus and continues around the inferior border of the hemisphere to form

the lateral part of the basal surface.

Fig.1: Lateral surface of Temporal Lobe

Inferior surface - The basal surfaces of the temporal and occipital lobes are formed

by the same gyri that continue from anterior to posterior across their uninterrupted

surface. From medial to lateral are the parahippocampal and occipitotemporal gyri

and the basal surface of the inferior temporal gyrus. The parahippocampal gyrus

extends backward from the temporal pole to the posterior margin of the corpus

callosum and thence on it continues posteriorly to blend into the isthmus of the

cingulate gyrus and the lingula.

5

The collateral sulcus begins near the occipital pole and extends anteriorly, parallel

and lateral to the calcarine sulcus. Posteriorly, it separates the lingula and

occipitotemporal gyrus, and anteriorly, it courses between the parahippocampal

and the occipitotemporal gyri. The occipitotemporal sulcus courses parallel and

lateral to the collateral sulcus and separates the occipitotemporal gyrus and basal

surface of the inferior temporal gyrus.

Medial surface – The medial surface of the temporal lobe is formed predominantly

by the rounded medial surfaces of the parahippocampal gyrus and uncus. It is

formed by three longitudinal strips of neural tissue, located one above the other,

which are interlocked with the hippocampal formation.

The most inferior strip is formed by the rounded medial edge of the

parahippocampal gyrus. The middle strip is formed by the dentate gyrus, a narrow

serrated strip of gray matter located on the medial surface of the hippocampal

formation. The superior strip is formed by the fimbria of the fornix. The

parahippocampal and dentate gyri are separated by the hippocampal sulcus. The

dentate gyrus and the fimbria are separated by the fimbriodentate sulcus.

6

The parahippocampal gyrus also extends around the lower border to form the

medial part of the basal surface of the temporal lobe, where it is separated from the

medially projecting uncus by the rhinal sulcus.

Fig 2: Medial surface of Temporal Lobe

Uncus, is the medially projecting anterior part of the parahippocampal gyrus.

When viewed from above or below, it has an angular shape with anterior and

posterior segments that meet at a medially directed apex.

Amygdaloid nucleus, so named because it resembles an almond is situated entirely

within uncus. It forms the anterior wall of the temporal horn. It fuses with the tip of

the tail of the caudate nucleus. The amygdala gives rise to the stria terminalis,

7

which courses between the thalamus and caudate nucleus deep to the

thalamostriate vein.

Hippocampus is a curved elevation of gray matter; approximately 5 cm long.It runs

along entire length of the medial part of floor of the temporal horn. The Dentate

gyrus runs along the medial edge of hippocampus. The hippocampus blends into

and forms the upper part of the posterior uncal segment.

The hippocampus, the parahippocampal gyrus and the dentate gyrus together form

the hippocampal formation. The hippocampus is divided into three parts: head,

body and tail. The head, directed anteriorly, has 3-4 digitations, resembling paw of

sea-horse; hence called “pes hippocampus”. The body of the hippocampus extends

along the medial part of the floor of the temporal horn, narrowing into the tail that

disappears as a ventricular structure.

The convex ventricular surface is covered with ependyma. Beneath this lies a thin

layer of white matter – alveus. The alveus consists of nerve fibers which originated

in the hippocampus. These fibers converge medially to form a bundle, viz. fimbria.

The fimbria becomes continuous with the crus of fornix.

8

Fig 3: Anatomy of Hippocampus

2.2 PHYSIOLOGY OF TEMPORAL LOBE:

Cyto-architectonically the human temporal lobe is divided into 10 Brodmann’s

Areas but there is a high likelihood to be many more. Apart from the eloquent

temporal cortex some key subcortical regions involved intimately with the

functioning of the temporal lobe include the Limbic system, Amygdala and the

Hippocampal formation.

The temporal lobe is involved in 3 core sensory functions:

(a) Processing auditory information and Language and interpretation of emotional

dimension of auditory stimuli

(b) Processing visual information with regards to object identification and

9

emotional aspect interpretation of visual stimuli

(c) Learning and memory

It is well known that the temporal cortex is mainly responsible for processing

primary auditory stimuli and their sensory and emotional aspects. The first step in

perception of auditory stimulus takes place in the primary auditory area in the

superior temporal gyrus(STG) corresponding to Brodman’s area 41 & 42. What

happens subsequently, to the perceived auditory stimulus is a matter of extensive

scientific research. Schirmer et al.45

proposed that processing and subsequent

perception of auditory information occurs along 3 streams in the human temporal

lobe:

(1) a posterior stream going through the superior temporal sulcus which subserves

sound embodiment;

(2) a ventral stream passing through the middle temporal gyrus for conceptual

processing of auditory stimuli and

(3) an anterior stream extending along the superior temporal gyrus upto the

temporal pole for the purpose of semantic processing.

Thus the temporal cortex is extensively involved not only in perception of auditory

stimulus but also in processing the different aspects of the auditory stimuli like

emotional and semantic processing. Regarding the interpretation of the emotional

10

component of the auditory information, the amygdala has been shown to play a

vital role in interpretation of emotional vocalizations. Several studies have shown

the amygdala to be activated by emotional vocalizations, more so specifically

emotional prosody of words and sentences.11,12,56

Literature has abundant examples of incriminating the temporal cortex in the

process of visual & emotional perception. Haxby et al.17

proposed a visual

perception model in which it is hypothesized that primary visual information is

initially processed in the primary visual area in the occipital cortex (V1) and then

transmitted along a ventral pathway leading from the visual cortex (V1) to the

inferior temporal gyrus (ITG). The Inferior temporal gyrus contains an area of

eloquent cortex known as the Fusiform Face Area (FFA) which primarily

subserves the function for recognizing faces and this process is enhanced when this

facial information has an added emotional component to it. So, it is pretty evident

that the temporal cortex has an important role in interpretation of visual stimuli.

With regards to the variety of visual stimuli that humans are encountered with, it is

not only necessary to interpret the visual stimulus, but also there is an adaptive and

evolutionary need to decode the emotional component of this visual information.

One of the key areas of the temporal lobe involved in decoding emotional facial

11

information is the amygdala. In 1939, Heinrich Kluver and Paul Bucy reported

from their animal experiments on monkeys that the amygdala seems to be

quintessential to perceive fearful signals. This finding was extrapolated to humans

by Lanteaume et al.26

who in their study were able to incite negative states like fear

and sadness via electro-physiologic stimulation of the amygdala. Several studies in

humans have proposed that the connections between the amygdala and the Face

Area(FFA) on the Inferior Temporal Gyrus is altered by emotional perception.8,34,53

With respect to the specific role of amygdale in emotional perception, it is

currently postulated that it is important in detecting “salience” which is meant to be

a general feature of emotion.1,39,41

The predominant function of amygdala is to

facilitate perception processing through reciprocal connections with the sensory

cortex53,54

. The output of the amygdala is streamed towards, both, the areas of the

brain that govern bodily responses to stimuli (through the endocrine system and

autonomic nervous system), and also to the primary and associative areas like the

extrastriate visual system, the Fusiform Face Area in Inferior Temporal Gyrus

(ITG) , and the primary auditory area in the superior temporal gyrus (STG).

The precise role of the temporal cortex and its associated structures in processing

visual information along with its emotional component has been extensively

studied in patients undergoing anterior temporal lobectomy (ATL) and amygdalo-

12

hippocampectomy(AH) for lesional epilepsy. ATL with AH is known to affect the

perception facial emotional recognition and emotional situational recognition.36

The proposed hypothetical explanation for this, is the reduced modulation of the

amygdala on the ventral visual processing pathway and in the case of recognition

of facial emotions, on the fusiform face area (FFA).

Thus, the summary of current literature points out that, the temporal cortex is

responsible to decode the sensory value of a visual stimulus and the amygdala is

responsible for decoding the attached emotional component of the visual stimulus.

Thus, we hypothesize that a person who has undergone anterior temporal

lobectomy, will have a deficit not only in recognizing faces but also in decoding

the emotional aspect of the facial information and the situations they are involved

in.

The left and right medial temporal systems are found to sub serve different types of

material-specific information, mostly in accordance with the pattern of cerebral

language dominance.6,30,33,52

Learning and retention of verbal materials is

associated with the left temporal memory system, and that of nonverbal materials

is associated with the right temporal memory system, assuming a left cerebral

language dominance.

13

Lee et al.27

surmised a meta-analysis of studies related to memory decline after

temporal lobe dysfunction and concluded that verbal memory is lateralized in the

left hemisphere and that verbal memory tasks are sensitive to left temporal

dysfunction. The data for lateralization of nonverbal memory in the right

hemisphere is not entirely conclusive but usually right temporal dysfunction

manifests as a decline in non verbal memory.

Jones-Gotman et al.24

reported that patients with left temporal epilepsy showed a

retention deficit for a word list, whereas those with right temporal epilepsy showed

impaired learning of a design list. Similar findings were reported by Baxendale et

al.2 who observed that patients with left hippocampal sclerosis performed more

poorly than those with right hippocampal sclerosis on immediate and delayed prose

recall.

The scope and severity of human memory decline resulting from a bilateral

resection of the temporal lobe can best be captured in the study of the noted patient

H.M.46

who became amnesic in 1953 as the result of this surgical procedure for

control of his seizures. The anterograde amnesia that he had presented with

manifested as a dramatically impaired capacity for learning new material, or for

recollecting events after a distraction.

14

In summary, the Left temporal lobe predominantly subserves auditory and verbal

memory and the Right temporal lobe serves the purposes of visual memory.

Multimodal perception and memory encoding is mainly accomplished by the

participation of both temporal lobes in concert.

2.3 Neuro-Cognitive implications of Anterior Temporal Lobectomy (ATL) :

Surgery is often considered as the treatment of choice for drug resistant temporal

lobe epilepsy. Anterior Temporal Lobectomy (ATL) with Amygdalo-

hippocampectomy is the most commonly performed epilepsy surgery in patients

with refractory temporal lobe epilepsy . ATL is generally considered a safe surgery

with long term clinically significant neuro-cognitive sequelae occurring in only a

small fraction of patients undergoing ATL.

Wiebe et al.55

reported an overall long term persistent neuro-cognitive disability in

about 2-3% of patients undergoing ATL and concluded that it was a safe surgical

procedure from a long term prospective. Nevertheless, ATL is not completely

devoid of neuro-cognitive risk. Several studies have reported both short term and

long term neuro-cognitive changes associated with ATL. These changes may at

times be serious enough to necessitate interventions and rehabilitative measures to

reduce the morbidity of patients in performing activities of daily living.

15

Measuring the effects of ATL on neuro-cognition in epilepsy patients poses certain

singular challenges. First and foremost epilepsy is not a uniform condition, but is

infact heterogeneous in terms of clinical, demographic, and etiologic dimensions.

Precise predictions of outcome after any surgical intervention cannot be

generalized and an individualistic approach has to be adopted for individual

patients defining both surgical risks and benefits taking into account both

neurologic and neuropsychological factors. Secondly, epilepsy by virtue of being a

chronic condition, itself carries the probability of cognitive decline and reduced

psychological, vocational and social performance and compromised quality of

life.10,20,49

For the above mentioned reasons, routine statistical tools provide an overall trend

towards a particular neuro-cognitive deficit or benefit. Some empirically based

techniques for calculating individual change, like the Reliability Change Index

(RCI) and Standardized Regression-Based (SRB) change scores provide more

accurate and dependable risk estimates as compared to other measures for

cognitive changes after epilepsy surgery, and are now considered as the yard stick

in monitoring neuro-cognitive change after epilepsy surgery.5,7,21,43,51

16

Impact of ATL on IQ and Cognitive function:

Several studies in literature have investigated the impact of temporal lobe resection

on IQ and cognitive outcomes. But with regards to short term cognitive outcomes

only a handful of studies are available. Lee et al.28

, in their study on short term

outcome of ATL on cognition found that 39% of patients in their series had

improvements in IQ. Sherman et al.48

conducted a meta-analysis of all published

literature regarding cognitive outcome after ATL, and they reported in their series

of a 16 % improvement in IQ and psychomotor speed. Hence it is almost uniformly

agreed to upon in literature that epilepsy surgery carries an inherent benefit of an

increased psychomotor and cognitive performance in the post-operative period.

The exact neuro-physiological basis for improvement in IQ is yet to be elucidated

but it has been postulated that improvement in IQ is a reflection of

reduction/elimination of seizures post-operatively. The improvement in IQ may

also be partly be explained by patients having a reduced intake of anti-epileptic

medications in the post-operative period, with literature replete with evidence of

obtunding effect of these medications on the neuro-cognitive functions.29,31

Impact of ATL on Musical abilities:

17

Cortical resection studies using patients with intractable temporal lobe

epilepsy have shown deficits in discrimination of various musical stimuli

following Right ATL but not Left ATL, suggesting that hemispheric

specialization for music may have greater involvement of the right hemisphere

as compared to the left hemisphere.25

Milner et al.32

reported in their study that

ability to appreciate musical attributes showed greater decline in patients

undergoing Right ATL as compared to Left ATL. Shankweiler et al.47

used

electronically generated pure tones and intonations with differing musical

attributes and reported that ability to discriminate the different parameters of music

showed greater decline in patients with Right ATL as compared to Left ATL.

However, Hanschen et al.16

in their study, suggested that the right hemisphere was

involved in appreciation of gross attributes of music and the left hemisphere was

involved for appreciating certain attributes of music like pitch and rhythm. In their

report, Hanschen et al. revealed impairment in rhythm discrimination, reading

musical notation and detailed musical analysis following left hemisphere

damage.

18

These seemingly contradictory results are attributable to inconsistent

definitions of “musical processing” and differences in the types of stimuli

employed. As with other forms of cognitive processing, differential

hemispheric participation may depend on specific computational requirements

for aspects of musical processing (discrimination vs. perception vs. judgment)

and which component of music is being processed (pitch, rhythm, tempo,

etc.). It is unlikely that perception of individual tones, pitches, three or four

note melodies, electronically-generated sounds or excerpts from musical

pieces require the same type of processing. Hence appreciation of music and its

finer attributes may infact be possible only by bi-hemispheric participation, with

the right and left temporal lobes working in tandem to achieve the end result.

Earlier studies have focused on post-operative examination without elucidating

the relationship between pre- and post-operative performance. The present

study addresses these issues by using a comprehensive standardized battery

of musical aptitude tests administered to unilateral temporal lobe epileptics

before and after anterior temporal lobectomy.

Impact of ATL on multi-modal perception:

19

The temporal lobe, by virtue of its extensive involvement in processing visual and

auditory stimuli, plays an important role in multi-modal perception like recognition

of faces, facial emotion perception and emotional situation recognition.

Dulay et al.9 reported that patients undergoing ATL may have a transiently reduced

ability to recognize familiar faces. They also found that patients with temporal

lobectomy had a reduced ability to interpret and adapt to various social situations

due to obtunding of emotional perception after resection of anterior temporal lobe.

Gosselin et al.14

in their study, concluded that facial emotion interpretation was

most probably represented in a multimodal fashion in both temporal lobes and

hence resection of one temporal lobe is unlikely to significantly affect the ability to

decode facial emotions.

Both Dulay et al.9 and Gosselin et al.

14 had reported a non-specific decline in

general emotion understanding and social adaptation of patients with ATL in the

first 6 months of follow-up. Till date no literature is available that has conclusively

reported the implications of ATL on emotional situation adaptation and emotional

situation recognition.

Impact of ATL on Memory:

20

Memory decline represents one of the primary neuropsychological morbidities of

ATL.6,52

The right and left temporal lobes are found to sub serve different types of

material specific information, mostly in accordance with the pattern of cerebral

language dominance. Learning and retention of verbal materials is associated with

the left temporal memory system, and that of nonverbal materials like visual and

facial information is associated with the right temporal memory system, assuming

a left cerebral language dominance.30,33

Lee et al.27

surmised a meta-analysis of studies related to memory decline after

temporal lobe dysfunction and concluded that verbal memory is lateralized in the

left hemisphere and that verbal memory tasks are sensitive to left temporal

dysfunction. The data for lateralization of nonverbal memory in the right

hemisphere is not entirely conclusive but usually right temporal dysfunction

manifests as a decline in non verbal memory.

Jones-Gotman et al.24

reported that patients with left temporal epilepsy showed a

retention deficit for a word list, whereas those with right temporal epilepsy showed

impaired learning of a design list. Similar findings were reported by Baxendale et

al.21

who observed that patients with left hippocampal sclerosis performed more

poorly than those with right hippocampal sclerosis on immediate and delayed prose

recall.

21

The scope and severity of human memory decline resulting from a bilateral

resection of the temporal lobe can best be captured in the study of the noted patient

H.M.46

who became amnesic in 1953 as the result of this surgical procedure for

control of his seizures. The anterograde amnesia that he had presented with

manifested as a dramatically impaired capacity for learning new material, or for

recollecting events after a distraction. Since then, much research effort has been

invested in examining the role played by the temporal lobe in human memory.

An impairment of verbal memory has consistently been associated with resection

of the left dominant temporal lobe, whereas nonverbal memory deficits have been

less reliably observed after resection from the right temporal lobe.37

Numerous

other studies supported the observations that resection from the left ATL is

associated with postoperative decline in learning or retention of various types of

verbal material including words 23

and prose.13

Saykin et al.44

in their study reported that patients with right ATL showed decline

in nonverbal memory but improvement in verbal memory whereas those patients

with left ATL showed a decline in verbal memory but improvement in nonverbal

memory.

22

Ivnik et al.22

concluded that left ATL was found to impair immediate recall for

verbal materials (California Verbal Learning Test and a low-imagery word-

recognition task) but at the same time enhance immediate recall for nonverbal

material (Facial Recognition Memory Test and a modified Corsi Block task).The

review of published literature provides clear data that Left temporal resection

affects verbal memory and right temporal resection predominantly affects non-

verbal memory.

From the above mentioned data, it is quite clear that surgery for epilepsy does

indeed result in a certain degree of neuro-cognitive change albeit the change be

either positive or negative. The exact mechanisms by which either deficit or benefit

over neuro-cognitive functions occur after ATL are still being elucidated. However

the evidence from literature can be utilized to formulate discussions regarding

operative risks with prospective patients willing to undergo surgery for epilepsy.

Despite literature having evidence in abundance with regards to the changes in

cognitive functions after epilepsy surgery, ATL still continues to be the most

common surgical procedure performed worldwide for refractory temporal lobe

epilepsy. One commonly observed chief motivator for patients to undergo epilepsy

surgery happens to be the social stigma aligned with seizures, as the dread of

potential post-operative cognitive decline is a far cry to the optimism the patient

23

has of leading a seizure free life. Other factors may include non-compliance to a

drug schedule or adverse effects of the anti-epileptic medications.

Most studies in literature that measure outcome after epilepsy surgery, the quality

of life profile and neuro-cognitive outcome are usually measured at 6 months to

one year post surgery. Following up these patients for longer intervals has

frequently shown that the neuro-cognitive functions for most patients will


comparable to pre-operative values. Grammaldo et al.15

, in their study found out

that those patients undergoing ATL, particularly on the left side, mainly showed

impairment in verbal memory at one year of follow-up. However, it was also found

during long term follow-up of 2-4 years, that a majority of those patients with such

an impairment at 1 year, did regain some or most of the lost function and return to

a level that was almost similar to the pre-operative baseline, resulting in a very

minimal difference pre- and postoperatively for the entire group.

In a similar study, Helmstaedter et al.18

reported that patients undergoing ATL had

memory deficits post surgery (at around 6 months – 1 year) but they also found that

24

such patients demonstrated a recovery of memory function at long-term follow-up

of around 2–10 years.

Hence it is well established from review of literature that epilepsy surgery may

lead to cognitive deficits or at times even improvements. Also well documented is

the fact that such deficits gradually improve over long term follow-up so that many

patients almost reach their pre-operative baseline values. Knowledge of the timing

of such deficits is essential, as earlier intervention can potentially lessen the burden

of such deficits on a patient's quality of life.

Research has demonstrated the benefits of early intervention in neurocognitive

treatment, especially in the case of preterm infants50

, cognitive decline35

, and

following traumatic brain injury.38

Similarly, early intervention with individual

and group based interventions is effective in diminishing the negative cognitive

effects of epilepsy surgery.19,40

However, there is no clear consensus regarding the best time interval for evaluating

neuro-cognitive function after epilepsy surgery to detect any impairments that may

exist so that such patients may be expeditiously directed toward the appropriate

cognitive rehabilitation therapy. Therefore, the aim of our study is to compare and

contrast the pre-operative neuropsychological profile in patients undergoing ATL

for epilepsy with immediate postoperative and early post-operative (at 3 months)

25

performance. We hypothesized that short-term evaluation beginning at six weeks

after resective epilepsy surgery would reveal early changes in neuro-cognitive

function that may help to identify patients who may need expeditious referral to

rehabilitation, which may ultimately influence decisions such as early return to

work or school.

26

3. AIMS & OBJECTIVES

The aim of our study is

1) To compare and contrast the pre-operative neuro-psychological profile in

patients undergoing ATL(Left + Right) for epilepsy with immediate postoperative

and early post-operative (at 3 months) performance.

2) To compare the neuro-psychological profile in the immediate postoperative

period and early postoperative period between patients who have undergone Right

ATL vs. patients who have undergone Left ATL.

27

4. MATERIALS & METHODS:

This is a prospective non-randomized observational study conducted at the

Department of Neurosurgery and Madhavan Nayar Center for Comprehensive

Epilepsy Care (RMNC), Sree Chitra Tirunal Institute for Medical Sciences &

Technology from June 2015 to August 2016. The Institutional Ethics Committee of

the Sree Chitra Tirunal Institute for Medical Sciences & Technology approved this

study and signed informed consent was obtained from all patients for inclusion.

Relevant data was de-identified for use in statistical analyses.

Twenty patients treated at our institute were considered for inclusion in this study.

The Inclusion Criteria were pre-defined as -

i) Medically refractory epilepsy of temporal origin with imaging features

suggestive of mesial temporal sclerosis and electro-clinical concordance

ii) Adults >18 years

iii) Normal vision and hearing pre-operatively

Patients with extra-temporal lobe epilepsy, defective vision and hearing, with IQ of

< 40, with h/o previous temporal lobe surgery and with post traumatic epilepsy

28

were excluded from this study. Patients considered for selective mesial temporal

lobe surgery were also excluded from this study.

All patients included in the study underwent a standard anterior temporal

lobectomy along with amygdalo-hippocampectomy (amygdala + anterior third of

hippocampus). The extent of resection of temporal neocortical structures was

approximately around 3cm from the temporal pole in the dominant hemisphere and

around 4.5cm in the non-dominant hemisphere.

All patients included in the study underwent a detailed neuro-psychological

evaluation by a licensed neuro-psychologist with special emphasis on emotional

and musical cognitive abilities. The neuropsychological evaluation was conducted

at three different intervals – pre-operative (before surgery); immediate post-

operative (around 10 days after the surgery) and around 3 months after the surgery.

The neuro-psychological evaluation consisted of a battery of tests, broadly

surmised under the following headings.

(a) Intelligence test

(b) Tests for musical abilities

29

(c) Test for facial recognition

(d) Test for facial emotion recognition

(e) Test for emotional situation recognition

(f) Test for Auditory and Verbal memory Both Immediate Recall (IR)

(g) Test for Visual memory and Delayed Recall (DR)

Intelligence Test

Wechsler Adult Intelligence Scale (WAIS)

Wechsler test is one of the most frequently used measures in neuropsychological

batteries. The purpose of the Wechsler Scale is to provide a general measure of

intelligence function. It is a core instrument, giving information about the overall

level of intellectual functioning and the presence or absence of significant

intellectual ability, and providing clues to altered functions.

The Wechsler Adult intelligence scale – 4th ed India, is the Indian adaptation of the

global counterpart. It provides subtest and composite scores that represent

intellectual functioning in specific cognitive domains, as well as a composite score

that represent general intellectual ability. The test results are coded and a

composite IQ score is arrived at.

30

Test for musical ability:

To assess the musical ability of the examinee, we designed and subsequently

validated a new test battery. This idea is imported from Seashore Measures of

musical talents and modified appropriately. This newly developed battery contains

four sub tests as follows.

Pitch subtest: Twenty pairs of tones are presented to the examinee; in each pair the

participant determines whether the second tone is higher or lower in pitch than the

first. Number of correct responses indicates the score.

Loudness subtest: Nineteen pairs of tones are presented. The participant indicates

for each pair whether the second tone is stronger or weaker than the first. Number

of correct responses indicates the score.

Rhythm subtest: Fifteen pairs of rhythmic patterns comprise the rhythm test. The

participant indicates whether the two patterns in each pairs are same or different.

Number of correct responses indicates the score.

Timbre subtest: This test consist of fifteen pairs of tones. In each pair the

participant judges whether the tones are the same or different in tone quality.

Number of correct responses indicates the score.

31

Test for Facial recognition:

Facial recognition test is used to assess the ability of the subject to retain and

reproduce facial memory. In this test, the examinee is shown a series of

photographs of faces, one at a time and asked to remember each one. The

examinee is then shown a second series of photographs of faces, one at a time, and

asked to identify each faces as either one that he/she was shown previously or if it

is a new one. Number of correct responses indicates the score.

The aim of this test is to identify the ability of the examinee to interpret different

facial emotions. In this test Examinee is shown the pictures of faces depicting

universally accepted six different emotions (anger, fear, sad, surprise, disgust &

happy) and asked identify different emotions. Number of correct responses

indicates the score.

In this test the examinee is presented 20 different pictures that carry different

emotional situations (happiness, sadness, fear and anger) in an equal number of

distributions. The task is to correctly identify the emotional situation depicted in

Test for Facial Emotion Recognition:

Test for emotional situation recognition:

32

the pictures, with the help of corresponding smiles. The examinee is not making

verbal comments only pointing the corresponding smiles. Number of correct

responses indicates the score.

Test for Auditory and Verbal Memory:

Rey’s Auditory Verbal Learning and Memory Test:

This test assesses immediate memory span and elicits retroactive and proactive

interference tendencies and short term and long term retention. The test consists of

two 15- items word list, List A for learning trials and List B for distraction trials

and a 30-item word list for recognition trial. List A is presented 5 times, always in

the same order, with an assessment of recall of each presentation. Then, list B is

presented once and recall is recorded. After this the subject is asked to recall list- A

without presenting it. Twenty minutes after the recall of list A, the subject is asked

to recall the list A again without presenting it. After this, the word from the

recognition list are presented and the subject is asked to say “yes” for the word that

were present in List A and “no” for the words that were not presented in list A.

33

Test for Visual Memory:

Rey – Complex figure test:

The Complex Figure Test assesses the visuo-spatial memory and constructional

ability. The test consists of a complex stimulus figure. The subject is asked to copy

the stimulus figure without revealing the fact that he/she is supposed to recall the

figure after few minutes. The subject is asked to do free hand drawing, without

using a ruler to draw. The immediate recall trial is administered 3 minutes after the

copy trial is completed. The intermediate time between copy and recall, the subject

is given a verbal distraction task. Thirty minutes after the copy trial, the subject is

asked to once again draw the complex figure from memory for assessing the

delayed recall.

Statistical Analysis:

Descriptive and inferential statistical analysis has been carried out in the present

study. Results on continuous measurements are presented on Mean ± SD (Min-

Max) and results on categorical measurements are presented in Number (%).

Significance is assessed at 5 % level of significance.

Student t test (two tailed, dependent) has been used to find the significance of

study parameters on continuous scale within each group.

34

Significant figures

+ Suggestive significance (P value: 0.05<P<0.10)

* Moderately significant (P value: 0.01<P ≤ 0.05)

** Strongly significant (P value: P≤0.01)

Statistical software: The Statistical software namely SAS 9.2, SPSS 15.0, Stata

10.1, MedCalc 9.0.1 , Systat 12.0 and R environment ver. 2.11.1 were used for

the analysis of the data.

5. OBSERVATIONS &

A total of 20 patients (12 male and

Lobectomy (ATL) at the Department of Neurosurgery,

for Medical Sciences & Technology between June 2015

were divided into groups according to

underwent left ATL, and nine patients (45%) underwent righ

Side

Left

Right

Total

OBSERVATIONS & RESULTS:

total of 20 patients (12 male and 8 female) underwent Anterior Temporal

Department of Neurosurgery, Sree Chitra Tirunal Institute

Technology between June 2015 - August 2016

according to the side of surgery. Eleven pat

derwent left ATL, and nine patients (45%) underwent right ATL.

Side No. of patients %

Left 11 55.0

Right 9 45.0

Total 20 100.0

55%

45%

Side

Left

Right

35

) underwent Anterior Temporal

Sree Chitra Tirunal Institute

August 2016. Patients

side of surgery. Eleven patients (55%)

Outcomes of the Neuro-psychological battery of tests

Intelligence Quotient (IQ):

In our study, as a whole, of the

the average IQ pre-operatively

operative period was 64.90

post-operatively was 68.20.

Variable

Pre-op

Imm.

post-op

3rd

mon.

post

IQ 61.70

(±22.42)

64.90

(±28.04)

68.20

(±28.59)

Preop

IQ 61.7

58

60

62

64

66

68

70

psychological battery of tests:

of the 20 patients who underwent ATL (left

eratively was 61.70. The mean IQ in the immediate post

64.90 and the average IQ during follow-up in the 3

mon.

post-op

Difference p

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

68.20

(±28.59)

+ 3.2 + 6.5 + 3.3 0.236

Preop Imm Post op 3rd month Postop

61.7 64.9 68.2

Mean IQ

36

L (left + right ATL),

The mean IQ in the immediate post-

up in the 3rd

month

p – Value

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

0.013 * 0.075 +

37

As compared to the pre-op values the mean IQ showed an increase of 3.2 (p value

= 0.236) in the immediate post-op period and in the 3rd

month post-op there was an

increase in mean IQ of 6.5 (p value = 0.013*) as compared to pre-op values. The

mean IQ showed an increase of 3.3 (p value = 0.075+) when the immediate post-op

values were compared to the 3rd

month post-op values.

The increase in IQ between pre-op to 3rd

month post-op was found statistically

significant (p value < 0.05). The increase in IQ between immediate post-op to 3rd

month post-op was found to be suggestive of significance statistically (p value <

0.10).

IQ change in Left ATL vs. Right ATL:

On evaluating the mean IQ levels in patients who underwent left ATL (n=11),

there was an increase in mean IQ of 8.0 (p value = 0.070+) in the 3

rd month post-op

period as compared to pre-op values. The mean IQ showed an increase of 6.27 (p

value = 0.031*) when the immediate post-op values were compared to the 3rd


Among patients who underwent right ATL (n=9), there was an increase of mean

IQ values by 5.0 (p value = 0.057 +) in the immediate post-op period and in the 3

rd

month post-op there was an increase in mean IQ of 4.67 (p value = 0.078+) as

compared to pre-op values.

38

IQ

Pre-op

Imm.

post-op

3rd

mon.

post-op

Difference p – Value

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL

55.36

(±20.79) 57.09

(±27.76)

63.36

(±29.45) + 1.727 + 8.000 + 6.273 0.706 0.070

+ 0.031*

Right

ATL 69.44

(±23.05)

74.44

(±26.79)

74.11

(±28.03) + 5.000 + 4.667 - 0.333 0.057

+ 0.078

+ 0.864

Hence it was found in our study that patients undergoing Left ATL had significant

improvement in the post-op IQ values(p value <0.05) at 3 months while patients

undergoing Right ATL had only a modest improvement of IQ in the post op period

(p value < 0.10).

Pre Op Imm Post Op 3rd month Post Op

Left ATL 55.36 57.09 63.36

Right ATL 69.44 74.44 74.11

40

50

60

70

80

90

Mean IQ : Left vs Right ATL

Test for Musical Ability – Pitch Recognition Subtest

In our study, the average pitch recognition score

mean pitch recognition score

during follow-up in the 3rd

score was 11.15.

Variable

Pre-op

Imm.

post-op

3rd

mon.

post

Pitch 11.05

(± 3.05)

11.40

(± 2.87)

11.15

(± 2.62

As compared to the pre-op values the

increase of 0.35 (p value = 0.548

month post-op there was an increase

value = 0.869) as compared to pre

Preop

Pitch 11.05

10

10.5

11

11.5

12

Pitch Recognition Subtest

In our study, the average pitch recognition score pre-operatively was

pitch recognition score in the immediate post-operative period was

rd month post-operatively the mean pitch recognition

mon.

post-op

Difference p

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

11.15

(± 2.62)

+ 0.35 + 0.10 - 0.25 0.548

op values the mean pitch recognition scores showed an

= 0.548) in the immediate post-op period and in the 3

there was an increase in mean pitch recognition scores

as compared to pre-op values.


11.05 11.4 11.15

Pitch Score

39

operatively was 11.05. The

operative period was 11.40 and

the mean pitch recognition

p – Value

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

0.869 0.685

pitch recognition scores showed an

op period and in the 3rd

in mean pitch recognition scores of 0.1 (p

3rd month Postop

40

The change in the pitch recognition scores between pre-op values and immediate

post-op values and 3rd

month post-op values were not found to be statistically

significant (p value > 0.10).

Pitch recognition score change in Left ATL vs. Right ATL:

On evaluating the mean pitch recognition scores in patients who underwent Left

ATL (n=11), there was an increase of 0.27 (p value = 0.720) in the immediate post-


month post-op, there was a decrease in the mean pitch

recognition scores of 0.27 (p value = 0.743) as compared to pre-op values. The

mean pitch recognition scores showed a decrease of 0.54 (p value = 0.493) when

the immediate post-op values were compared to the 3rd



pitch recognition scores by 0.44 (p value = 0.650) in the immediate post-op period

and in the 3rd

month post-op, there was an increase in the mean pitch recognition of

0.55 (p value = 0.560) as compared to pre-op values. The mean pitch recognition

scores showed a slight increase of 0.11 (p value = 0.915) when the immediate post-

op values were compared to the 3rd


41

Pitch

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 12.00

(±2.90)

12.27

(±3.13)

11.73

(±1.85) +0.273 -0.273 -0.545 0.720 0.743 0.493

Right

ATL 9.89

(±2.98)

10.33

(±2.24)

10.44

(±3.32) +0.444 +0.556 +0.111 0.650 0.560 0.915

The change in the pitch recognition scores between pre-op values and immediate


month post-op values in patients undergoing Left ATL vs.

Right ATL was not found to be statistically significant (p value > 0.10).

Test for Musical Ability – Rhythm Recognition Subtest

In our study, the average rhythm recognition score pre-operatively was 14.20. The

mean rhythm recognition score in the immediate post-operative period was 13.80


Left ATL 12 12.27 11.73

Right ATL 9.89 10.33 10.44

8

9

10

11

12

13

14

Mean Pitch Score : Left vs Right ATL

and during follow-up in the 3

score was 13.40.

Variable

Pre-op

Imm.

post-op

3rd

mon.

post

Rhythm 14.20

(±1.58)

13.80

(±1.67)

13.40

(±1.93)


decrease of 0.40 (p value = 0.379

month post-op, there was a de

value = 0.061+) as compared to pre

Rhythm

12.5

13

13.5

14

14.5

15

up in the 3rd

month post-operatively the mean pitch recognition

mon.

post-op

Difference p

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

13.40

(±1.93) 0.400 0.800 0.400 0.379

op values the mean rhythm recognition scores showed a

= 0.379) in the immediate post-op period and

, there was a decrease in mean rhythm recognition scores



14.2 13.8 13.4

Rhythm Score

42

the mean pitch recognition

p – Value

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

0.061+ 0.278

mean rhythm recognition scores showed a

period and in the 3rd

in mean rhythm recognition scores of 0.80 (p

3rd month Postop

43

The change in the rhythm recognition scores between pre-op values and 3rd

month

post-op values were suggestive of significance statistically (p value < 0.1).

Rhythm recognition score change in Left ATL vs. Right ATL:

On evaluating the mean rhythm recognition scores in patients who underwent left

ATL (n=11), there was a decrease of 0.72 (p value = 0.16) in the immediate post-


month post-op, there was a decrease in the mean rhythm

recognition scores of 1.45 (p value = 0.020*) as compared to pre-op values.

Among patients who underwent right ATL (n=9), there was a decrease of mean

rhythm recognition scores by 0.20 (p value = 0.780) in the immediate post-op


month post-op, there was an increase in the mean rhythm

recognition values of 0.02 (p value = 0.960) as compared to pre-op values.

Rhythm

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 14.55

(±1.75)

13.82

(±1.66)

13.09

(±2.21) -0.727 -1.455 -0.727 0.167 0.020* 0.195

Right

ATL 13.78

(±1.30)

13.58

(±1.79)

13.80

(±1.56) -0.20 +0.002 +0.22 0.780 0.960 0.615

44

In our study, we found that in patients undergoing Left ATL, there was a

statistically significant (p value <0.05) fall in rhythm recognition scores between

pre-op and 3rd

month post op values. The change in the rhythm recognition scores

in patients undergoing Right ATL between pre-op, immediate post-op and 3rd

month post-op was not found to be statistically significant.

Test for Musical Ability – Timbre Recognition Subtest

In our study, the average timbre recognition score pre-operatively was 13.50. The

mean timbre recognition score in the immediate post-operative period was 13.50

and during follow-up in the 3rd

month post-operatively the mean timbre recognition

score was 13.30.


Left ATL 14.55 13.82 13.09

Right ATL 13.78 13.58 13.8

12

12.5

13

13.5

14

14.5

15

Mean Rhythm Score : Left vs Right ATL

Variable

Pre-op

Imm.

post-op

3rd

mon.

post

Timbre 13.50

(±1.64)

13.50

(±1.61)

13.30

(±1.38)


change in the immediate post

decrease in mean timbre recognition scores

pre-op values.

The change in the timbre recognition scores between pre


month post


Timbre

12.5

13

13.5

14

14.5

mon.

post-op

Difference p

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

13.30

(±1.38) 0.000 -0.200 -0.200 1.000

op values the mean timbre recognition scores showed no

post-op period and in the 3rd

month post-op

in mean timbre recognition scores of 0.2 (p value = 0.869) as compared to

recognition scores between pre-op values and immediate

month post-op values were not found to be statistically


13.5 13.5 13.3

Mean Timbre Score

45

p – Value

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

0.645 0.606

mean timbre recognition scores showed no

op there was a

as compared to

op values and immediate

op values were not found to be statistically

3rd month Postop

46

Timbre recognition score change in Left ATL vs. Right ATL:

On evaluating the mean timbre recognition scores in patients who underwent Left

ATL (n=11), there was a decrease of 0.45 (p value = 0.395) in the immediate post-


month post-op, there was a decrease in the mean timbre

recognition scores of 0.909 (p value = 0.074+) as compared to pre-op values.

Among patients who underwent Right ATL (n=9), there was an increase of mean

timbre recognition scores by 0.55 (p value = 0.302) in the immediate post-op


month post-op, there was an increase in the mean timbre

recognition of 0.66 (p value = 0.360) as compared to pre-op values.

Timbre

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 13.73

(±0.90)

13.27

(±1.90)

12.82

(±1.66) -0.455 -0.909 -0.455 0.395 0.074+ 0.501

Right

ATL 13.22

(±2.28)

13.78

(±1.20)

13.89

(±0.60) +0.556 +0.667 +0.111 0.302 0.360 0.729

In our study, we found that in patients undergoing Left ATL, there was a fall of

timbre recognition scores between pre-op and 3rd

month post-op values which was

suggestive of significance statistically (p value <0.10). The change in the timbre

recognition scores in patients undergoing Right ATL between pre-op, immediate

47

post-op and 3rd

month post-op was not found to be statistically significant (p value

> 0.10.

Test for Musical Ability – Loudness Recognition Subtest:

In our study, the average loudness recognition score pre-operatively was 18.05.

The mean loudness recognition score in the immediate post-operative period was

17.45 and during follow-up in the 3rd

month post-operatively the mean loudness

recognition score was 18.15.

Variable

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Loudness 18.05

(±1.70)

17.45

(±2.33)

18.15

(±1.39) -0.600 +0.100 +0.700 0.293 0.821 0.217


Left ATL 13.73 13.27 12.82

Right ATL 13.22 13.78 13.89

12

12.5

13

13.5

14

14.5

15

Mean Timbre Score : Left vs Right ATL


decrease of 0.6 (p value = 0.293)

month post-op there was an in

value = 0.821) as compared to pre

The change in the loudness

immediate post-op values and 3

statistically significant (p value > 0.10).

Loudness recognition score

On evaluating the mean loudness

Left ATL (n=11), there was a

post-op period and in the 3

Loudness

16

16.5

17

17.5

18

18.5

19

Mean Loudness Score

op values the mean loudness recognition scores showed a

rease of 0.6 (p value = 0.293) in the immediate post-op period

there was an increase in mean loudness recognition scores


ange in the loudness recognition scores between pre-op values and

op values and 3rd

month post-op values were not found to be


recognition score change in Left ATL vs. Right ATL:

evaluating the mean loudness recognition scores in patients who underwent

eft ATL (n=11), there was a decrease of 1.63 (p value = 0.03*) in the immediate

and in the 3rd

month post-op, there was a decrease


18.05 17.45 18.15

Mean Loudness Score

48

mean loudness recognition scores showed a


in mean loudness recognition scores of 0.1 (p

op values and

op values were not found to be

recognition scores in patients who underwent

in the immediate

crease in the mean

3rd month Postop

49

loudness recognition scores of 0.18 (p value = 0.64) as compared to pre-op values.


loudness recognition scores by 0.67 (p value = 0.397) in the immediate post-op


month post-op, there was an increase in the mean loudness

recognition of 0.44 (p value = 0.622) as compared to pre-op values.

Loudness

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left ATL 18.18

(±1.47)

16.55

(±2.62)

18.00

(±1.41) -1.636 -0.182 +1.455 0.036* 0.640 0.120

Right

ATL 17.89

(±2.03)

18.56

(±1.33)

18.33

(±1.41) +0.667 +0.444 -0.222 0.397 0.622 0.681


Left ATL 18.18 16.55 18

Right ATL 17.89 18.56 18.33

16

16.5

17

17.5

18

18.5

19

Mean Loudness Score : Left vs Right ATL

50


loudness recognition scores between pre-op and immediate post-op values which

was statistically significant (p value <0.05). However the loudness recognition

score returned to near pre-op baseline value in the 3rd

month post-op follow-up.

The change in the loudness recognition scores in patients undergoing Right ATL

between pre-op, immediate post-op and 3rd

month post-op were not found to be


Facial Recognition:

In our study, the average facial recognition score pre-operatively was 33.5. The

mean facial recognition score in the immediate post-operative period was 35.75

and during follow-up in the 3rd

month post-operatively the mean facial recognition

score was 36.50.

Variable

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Facial

Recogn

33.55

(±5.08)

35.75

(±4.55)

36.50

(±5.39) +2.200 +2.950 +0.750 0.051+ 0.007** 0.428

As compared to the pre-op values the mean facial recognition scores showed an

increase of 2.2 (p value = 0.051+) in the immediate post-op period and in the 3

rd

month post-op there was an in

value = 0.007**) as compared to pre

The change in the facial recognition scores between pre

post-op values was suggestive of significance

in the facial recognition scores between pre

was found to be strongly significant statistically (p value <

Facial recognition score change in Left ATL

On evaluating the mean facial recognition scores in patients who underwent Left

ATL (n=11), there was an in


month post

recognition scores of 3.0 (p value

Facial Recognition

33.5

34.5

35.5

36.5

Facial Recognition Score

there was an increase in mean facial recognition scores


The change in the facial recognition scores between pre-op values and immediate

was suggestive of significance(p value < 0.10), whereas the change

in the facial recognition scores between pre-op values and 3rd

month post

was found to be strongly significant statistically (p value < 0.01).

change in Left ATL vs. Right ATL:


n increase of 1.36 (p value =0.34) in the immediate

month post-op, there was an increase in the mean facial

(p value = 0.074+) as compared to pre-op values

Preop Imm Post op3rd month

Postop

Facial Recognition 33.55 35.75 36.5

33

33.5

34

34.5

35

35.5

36

36.5

37

Facial Recognition Score

51

recognition scores of 2.95 (p

and immediate

, whereas the change

month post-op values


in the immediate post-

in the mean facial

op values.

52


facial recognition scores by 3.2 (p value = 0.089+) in the immediate post-op period

and in the 3rd

month post-op, there was an increase in the mean facial recognition

of 2.8(p value = 0.048*) as compared to pre-op values.

Facial

Recogn

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 33.55

(±4.7)

34.91

(±4.04)

36.55

(±5.97) +1.364 +3.000 +1.636 0.343 0.074+ 0.143

Right

ATL 33.56

(±5.81)

36.78

(±5.17)

36.44

(±4.93) +3.222 +2.889 -0.333 0.089+ 0.048* 0.843

In our study, we found that in patients undergoing Left ATL, the increase in facial

recognition scores between pre-op and 3rd

month post-op was suggestive of


Left ATL 33.55 34.91 36.55

Right ATL 33.56 36.78 36.44

33

33.5

34

34.5

35

35.5

36

36.5

37

Facial Recognition Score : Left vs Right ATL

53

significance statistically (p value <0.10). The increment in the facial recognition

scores in patients undergoing Right ATL between pre-op to immediate post-op was

suggestive of significance statistically (p value <0.10) while the increase in scores

between pre-op and 3rd

month post-op was found to be statistically significant

(<0.05).

Facial Emotion Recognition:

In our study, the average facial emotion recognition score pre-operatively was

5.25. The mean facial emotion recognition score in the immediate post-operative

period was 4.80 and during follow-up in the 3rd

month post-operatively it was 4.85.

Variable

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Facial

Emotion

Recogn

5.25

(±1.07)

4.80

(±1.67)

4.85

(±1.46) -0.450 -0.400 +0.050 0.176 0.104 0.883

As compared to the pre-op values the mean facial emotion recognition scores

showed a decrease of 0.45 (p value = 0.17) in the immediate post-op period and

in the 3rd

month post-op there was a decrease in mean facial emotion recognition

scores of 0.40 (p value = 0.104) as compared to pre-op values.

The change in the facial emotion recognition scores between pre



Facial emotion recognition score

On evaluating the mean facial emotion recognition scores in patients who

underwent Left ATL (n=11), there was a de

immediate post-op period and in the 3

mean facial emotion recognition scores of

pre-op values.

Among patients who underwent right ATL (n=9), there was

facial emotion recognition scores by

Facial emoticon

recognition

4

4.5

5

5.5

6

Facial Emotion Recognition Score

The change in the facial emotion recognition scores between pre-

op values and 3rd

month post-op values were not found to be




underwent Left ATL (n=11), there was a decrease of 0.72 (p value

and in the 3rd

month post-op, there was a de

mean facial emotion recognition scores of 0.18 (p value = 0.50) as compared to

Among patients who underwent right ATL (n=9), there was a decrease of

facial emotion recognition scores by 0.11(p value = 0.81) in the immediate

Preop Imm Post op3rd month

Postop

Facial emoticon

recognition5.25 4.8 4.85

4

4.5

5

5.5

6

Facial Emotion Recognition Score

54

-op values and

op values were not found to be

Right ATL:


= 0.13) in the

there was a decrease in the

as compared to

crease of mean

in the immediate post-op

55


month post-op, there was a decrease in the mean facial

emotion recognition of 0.67 (p value = 0.14) as compared to pre-op values.

Facial

Emotion

Recogn

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 5.18

(±1.17)

4.45

(±2.02)

5.00

(±1.55) -0.727 -0.182 +0.545 0.136 0.506 0.052+

Right

ATL 5.33

(±1.00)

5.22

(±1.09)

4.67

(±1.41) -0.111 -0.667 -0.556 0.813 0.141 0.416

In our study, we found that in patients undergoing both Left ATL and Right ATL,

the change in the facial emotion recognition scores were not found to be

statistically significant.


Left ATL 5.18 4.45 5

Right ATL 5.33 5.22 4.67

4

4.5

5

5.5

6

Facial Emotion Recognition Score : Left vs Right ATL

56

Emotion Situation Recognition:

In our study, the average emotion situation recognition score pre-operatively was

17.5. The mean emotion situation recognition score in the immediate post-

operative period was 17.85 and during follow-up in the 3rd

month post-operatively

the mean emotion situation recognition score was 18.85.

Variable

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Emotion

Situtn

Recogn

17.50

(±3.00)

17.85

(±3.00)

18.85

(±1.81) +0.350 +1.350 +1.000 0.569 0.007** 0.035*

As compared to the pre-op values the mean emotion situation recognition scores

showed an increase of 0.35 (p value = 0.56) in the immediate post-op period and in

the 3rd

month post-op there was an increase in mean emotion situation recognition

scores of 1.35 (p value = 0.0.007**) as compared to pre-op values. There was an

increase of 1.0 in the 3rd

month post-op scores as compared to immediate post-op

The increase in the emotion situation recognition scores between pre-op values and

3rd

month post-op values was found to be strongly significant statistically (p value

< 0.01), while the increase in the emotion situation recognition scores between

values (p value = 0.035*)


moderately significant statistically

Emotion situation recognition score

On evaluating the mean emotion situation recognition scores in patients who

underwent Left ATL (n=11), there was a

0.87) in the immediate post

increase in the mean emotion situation recognition scores

0.014*) as compared to pre

scores showed an increase of 1.27

values were compared to 3rd

Among patients who underwent right ATL (n=9), there was

emotion situation recognition scores by

Emotional situation

recognition

17

17.5

18

18.5

19

19.5

Emotion Situation Recognition Score

op values and 3rd

month post-op values was foun

statistically (p value < 0.05).



underwent Left ATL (n=11), there was a marginal decrease of 0.091


month post-op,

in the mean emotion situation recognition scores of 1.18

compared to pre-op values. The mean emotion situation recognition

of 1.27 (p value = 0.040*) when the immediate post

to 3rd month post-op.

Among patients who underwent right ATL (n=9), there was an increase of

n recognition scores by 0.89 (p value = 0.45) in the immediate


17.5 17.85 18.85

Emotion Situation Recognition Score

57

op values was found to be

Right ATL:


0.091 (p value =

op, there was an

of 1.18 (p value =

. The mean emotion situation recognition

) when the immediate post-op

an increase of mean

in the immediate

3rd month Postop

18.85

58


month post-op, there was an increase in the mean

emotion situation recognition of 1.5 (p value = 0.116) as compared to pre-op

values.

Emotion

Situtn

Recogn

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 17.73

(±2.65)

17.64

(±3.50)

18.91

(±2.17) -0.091 +1.182 +1.273 0.887 0.014* 0.040*

Right

ATL 17.22

(±3.53)

18.11

(±2.42)

18.78

(±1.39) +0.889 +1.556 +0.667 0.452 0.116 0.397

In our study, we found that in patients undergoing Left ATL, there was an increase

in the emotion situation recognition scores between pre-op and 3rd

month post-op

values and a similar increase between immediate post-op and 3rd

month post-op

values which was statistically significant (p value <0.05). The change in the


Left ATL 17.73 17.64 18.91

Right ATL 17.22 18.11 18.78

17

17.5

18

18.5

19

19.5

Emotion Situation Recognition Score : Left vs Right ATL

59

emotion situation recognition scores in patients undergoing Right ATL between

pre-op, immediate post-op and 3rd

month post-op were not found to be statistically


Auditory and Verbal Memory:

In our study, the average auditory and verbal memory score on immediate recall

(IR) pre-operatively was 8.95. The mean auditory and verbal memory score (IR) in

the immediate post-operative period was 8.65 and during follow-up in the 3rd


The average auditory and verbal memory score on delayed recall (DR) pre-

operatively was 8.65. The mean auditory and verbal memory score (DR) in the

immediate post-operative period was 8.50 and during follow-up in the 3rd

month

post-operatively it was 10.10.

Auditory

&

Verbal

Memory

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

IR 8.95

(±3.35)

8.65

(±4.31)

9.90

(±3.88) 0.300 -0.950 -1.250 0.639 0.033* 0.056+

DR 8.65

(±3.38)

8.50

(±4.61)

10.10

(±3.40) 0.150 -1.450 -1.600 0.851 0.024* 0.058+


(IR) showed an increase of 0.95 (p value = 0.03*) in the 3

There was an increase of 1.25 (p value = 0.056

Preop

AVL DR 8.65

8

8.5

9

9.5

10

10.5

Auditory & Verbal Memory: Delayed Recall

Preop

AVL IR 8.95

8

8.5

9

9.5

10

10.5

Auditory & Verbal Memory: Immediate Recall

compared to immediate post

op values the mean auditory and verbal memory scores

(IR) showed an increase of 0.95 (p value = 0.03*) in the 3rd

month post

There was an increase of 1.25 (p value = 0.056+) in the 3

rd month post


8.65 8.5 10.1



8.65 9.9


compared to immediate post-op scores.

60

mean auditory and verbal memory scores

post-op period.

month post-op scores as

3rd month Postop

10.1


3rd month Postop

9.9


61

When compared with the pre-op values the mean auditory and verbal memory

scores (DR) showed an increase of 1.45 (p value = 0.024*) in the 3rd

month post-op

period. There was an increase of 1.60 (p value = 0.058+) in the 3

rd month post-op

scores as compared to immediate post-op scores.

The improvement in auditory and verbal memory for both immediate recall and

delayed recall between pre-op values and 3rd

month post-op values was found to be

statistically significant (p value < 0.05), while the increase in the auditory and

verbal memory scores for both immediate and delayed recall between immediate


month post-op values was found to be suggestive of

statistical significance (p value < 0.10).

Auditory and Verbal Memory change in left ATL vs. Right ATL:

On evaluating the average auditory and verbal memory scores (both IR+DR) in

patients who underwent Left ATL (n=11), there was a decrease of 1.9 (p value =

0.02*) in the immediate post-op period and in the 3rd

month post-op, these values

reached almost pre-op values with a marginal difference of 0.45 (p value = 0.5).

Among patients who underwent Right ATL (n=9), there was an increase of the

average auditory and verbal memory scores (both IR+DR) by 1.4 (p value = 0.05*)

62

in the immediate post-op period and in the 3rd

month post-op, there was an increase

of 1.5 (p value = 0.028*) as compared to pre-op values.

Auditory

&

Verbal

Memory

(IR+DR)

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 11.55

(±2.25)

9.64

(±3.35)

11.09

(±2.81) 1.909 0.455 -1.455 0.028* 0.567 0.058+

Right

ATL 10.56

(±3.28)

12.00

(±3.67)

12.33

(±2.69) -1.444 -1.778 -0.333 0.050+ 0.028* 0.700


Auditory and Verbal Memory in the immediate post-op period (p value < 0.05)

which gradually improved and reached almost pre-op baseline levels by the 3rd


Left ATL 11.55 9.64 11.09

Right ATL 10.56 12 12.33

9

10

11

12

13

Auditory & Verbal Memory: Left vs Right ATL

63

month post-op follow-up. In patients undergoing Right ATL, the Auditory and

verbal memory scores improved in the immediate post-op period as well as in the

3rd

month post op both of which were statistically significant (p value < 0.05).

Visual Memory:

In our study, the visual memory score on immediate recall (IR) pre-operatively was

14.13. The mean visual memory score (IR) in the immediate post-operative period

was 19.0 and during follow-up in the 3rd


The average visual memory score on delayed recall (DR) pre-operatively was

14.15. The mean visual memory score (DR) in the immediate post-operative period

was 18.28 and during follow-up in the 3rd


Visual

Memory

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

IR 14.13

(±8.39)

19.00

(±7.79)

22.58

(±7.32) +4.875 +8.450 +3.575 0.004** <0.001** 0.007**

DR 14.15

(±8.94)

18.28

(±8.16)

20.58

(±9.02) +4.125 +6.425 +2.300 0.017* <0.001** 0.137

As compared to the pre-op values the mean visual memory scores (IR) showed an

increase of 4.8 (p value = 0.004**) in the immediate post-op period and in the 3rd

month post-op period there was an increase of 8.45 (p value < 0.001**).


increase of 4.12 (p value = 0.017*) in the immediate post

month post-op period there was an increase of 6.42 (p value < 0.001**).

Visual Memory IR

13

14

15

16

17

18

19

20

21

22

23

Visual Memory: Immediate Recall

Visual Memory DR

13

14

15

16

17

18

19

20

21

Visual Memory: Delayed Recall

op values the mean visual memory scores (DR) showed an

increase of 4.12 (p value = 0.017*) in the immediate post-op period and in the 3

there was an increase of 6.42 (p value < 0.001**).


14.13 19 22.58

Visual Memory: Immediate Recall


14.15 18.28 20.58

Visual Memory: Delayed Recall

64

mean visual memory scores (DR) showed an


there was an increase of 6.42 (p value < 0.001**).

3rd month Postop

22.58

3rd month Postop

20.58

65

The improvement in visual memory for both immediate recall and delayed recall

between pre-op and immediate post-op period was significant statistically (p <

0.05) whereas the increase in visual memory scores between pre-op values and 3rd

month post-op values was found to be strongly significant statistically (p value <

0.01).

Visual Memory change in left ATL vs. Right ATL:

On evaluating the average visual memory scores (IR) in patients who underwent

Left ATL (n=11), there was an increase of 3.6 (p value = 0.093+) in the immediate


month post-op, these values further increased by 9.3

(p value = 0.003**). The mean visual memory scores (DR) in patients who

underwent Left ATL (n=11) showed an increase of 2.5 (p value = 0.271) in the

immediate post-op period and in the 3rd

month post-op, these values further

Among patients who underwent Right ATL (n=9), the average visual memory

scores (IR) showed an increase of 6.38 (p value = 0.02*) in the immediate post-op


month post-op, these values further increased by 7.33 (p value

= 0.006**). The mean visual memory scores (DR) in patients who underwent

Right ATL (n=9) showed an increase of 6.0 (p value = 0.026*) in the immediate

increased by 7.63 (p value = 0.003**).

66


month post-op, these values showed an improvement

of 4.9 (p value = 0.024*).

Visual

Memory

(IR)

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 15.05

(±7.80)

18.68

(±6.5)

24.41

(±5.36) +3.636 +9.364 +5.727 0.093+ 0.003** 0.003**

Right

ATL 13.00

(±9.41)

19.39

(±9.55)

20.33

(±9.01) +6.389 +7.333 +0.944 0.023* 0.006** 0.572

Visual

Memory

(DR)

Pre-op

Imm.

post-op

3rd

mon.

post-op


Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Pre-op

to

Imm.

post-op

Pre-op

to

3rd

mon.

post-op

Imm.

post-op

to

3rd

mon.

post-op

Left

ATL 15.55

(±8.36)

18.09

(±7.0)

23.18

(±5.40) +2.545 +7.636 +5.091 0.271 0.002** 0.011*

Right

ATL 12.44

(±9.82)

18.50

(±9.84)

17.39

(±11.66) +6.056 +4.944 -1.111 0.026* 0.024* 0.625

In our study, we found that in patients undergoing Left ATL (n=11), the visual

memory scores (IR) showed an improvement in the immediate post-op period that

was suggestive of significance (p value < 0.10). It was also noted that this

improvement in visual memory score (IR) further improved in the 3rd

month post-

op period which was strongly significant statistically (p value < 0.01).

In these patients with Left ATL (n=11), the visual memory scores (DR) showed

improvement in the 3rd

month post-op which was strongly significant statistically

(p value < 0.01).

67


Left ATL 15.05 18.68 24.41

Right ATL 13 19.39 20.33

11

12.5

14

15.5

17

18.5

20

21.5

23

24.5

Visual Memory Immediate Recall :

Left vs Right ATL


Left ATL 15.55 18.09 23.18

Right ATL 12.44 18.5 17.39

11

12.5

14

15.5

17

18.5

20

21.5

23

24.5

Visual Memory Delayed Recall :

Left vs Right ATL

68

Among patients undergoing Right ATL (n=9), the visual memory scores (IR)

showed an improvement in the immediate post-op period that was significant

statistically (p value < 0.05). It was also noted that this improvement in visual

memory score (IR) further improved in the 3rd

month post-op period which was

Among these patients with Right ATL (n=9), the visual memory scores (DR)

showed improvement, both in the immediate post-op period as well as in the 3rd

month post-op period which was significant statistically (p value < 0.05).

strongly significant statistically (p value < 0.01).

69

6. DISCUSSION

Literature is replete with evidence in abundance with regards to the neuro-

cognitive changes after epilepsy surgery. Despite this, ATL still continues to be the

most common surgical procedure performed worldwide for refractory temporal

lobe epilepsy.

In most of the studies that measure outcome after epilepsy surgery, the quality of

life profile and neuro-cognitive outcome are usually measured at 6 months to one

year post surgery. Long term follow-up of patients undergoing epilepsy surgery

has frequently shown that the neuro-cognitive deficits in most patients will


comparable to pre-operative values.15,18

Knowledge of the timing of neuro-cognitive deficits after epilepsy surgery is

essential, as earlier intervention can potentially lessen the burden of such deficits

on a patient's quality of life. However, there is no clear consensus regarding the

best time interval for evaluating neuro-cognitive function after epilepsy surgery. In

our present study, the pre-operative neuropsychological profile in patients

undergoing Anterior Temporal Lobectomy (ATL) for epilepsy was compared with

immediate postoperative and early post-operative (at 3 months) performance to

evaluate the short term neuro-cognitive outcome after ATL.

70

Our study was a prospective non-randomized observational model in which 20

patients (12 male and 8 female) undergoing ATL and fulfilling the study inclusion

criteria were evaluated with a neuro-psychological battery of tests. The main aim

of the study was to assess the neuro-cognitive outcome after epilepsy surgery in the

short term (3 months post op) as well as to find any difference in neuro-cognitive

outcome between Left ATL vs. Right ATL.

In our study eleven patients (55%) underwent left ATL, and nine patients (45%)

underwent right ATL.

IQ outcome:

In our study, as a whole (Left + Right ATL), there was an increase in the IQ score

after ATL. The increase in IQ between pre-op to 3rd

month post-op was found

statistically significant (p value < 0.05) while the increase in IQ between

immediate post-op to 3rd

month post-op was found to be suggestive of significance


It was also found in our study that patients undergoing Left ATL had significant

improvement in the post-op IQ values (p value <0.05) at 3 months while patients

undergoing Right ATL had only a modest improvement of IQ in the post op period

at 3 months follow-up (p value < 0.10). Hence our study shows that post ATL,

71

there is an improvement of IQ with patients undergoing Left ATL having a greater

increment in IQ post operatively as compared to patients with Right ATL.

These findings correlate with that of Lee et al.28

who found that 39% of patients in

their series had improvements in IQ. Our findings are also concordant with those

of Sherman et al.48

who reported in their series of 16 % improvement in IQ and

psychomotor speed.

The exact neuro-physiological basis for improvement in IQ is yet to be elucidated

but it has been postulated that improvement in IQ is a reflection of

reduction/elimination of seizures post-operatively. The improvement in IQ may

also be partly be explained by patients having a reduced intake of anti-epileptic

medications in the post-operative period, with literature replete with evidence of

obtunding effect of these medications on the neuro-cognitive functions.29,31

Outcome of tests for Musical ability:

In our study, the ability to appreciate music was assessed by evaluating 4

parameters viz. Pitch, Rhythm, Timbre & Loudness.

In our study, overall (Left + Right ATL) the change in the pitch, rhythm, timbre &

loudness recognition scores between pre-op values and immediate post-op values

and 3rd

month post-op values were not found to be statistically significant (p value

> 0.10).

72

However on further analysis, we found that there was a significant decrease (p

value < 0.05) in the rhythm, timbre and loudness recognition scores between pre-

op values and 3rd

month post-op values in patients who underwent Left ATL. The

change in the rhythm, timbre and loudness recognition scores in patients

undergoing Right ATL between pre-op, immediate post-op and 3rd

month post-op

was not found to be statistically significant (p value > 0.10).

Our study results indicate that, patients who undergo Left ATL have deficits in

musical abilities in the paradigm of appreciating the rhythm, timbre and loudness

of music. However the durability and persistence/improvement of such deficits

need long term follow-up evaluation to arrive at any definitive conclusions.

Our findings are similar to those of Hanschen et al.16

who had reported in their

study that the right hemisphere was involved in appreciation of gross attributes of

music and the left hemisphere was involved for appreciating certain attributes of

music like pitch and rhythm. In their report, Hanschen et al.16

had also revealed

impairment in rhythm discrimination, reading musical notation and detailed

musical analysis following left hemisphere damage.

73

Even though Kester et al.25

have reported that musical ability is predominantly a

function of the right temporal lobe, the possible explanation for the contrasting

findings in our study is that due to functional re-organization of the right

hemisphere in chronic epilepsy patients, the impact of right ATL may not be as

profound as expected on appreciation of musical abilities. However, due to

language lateralization to the left hemisphere, the impact of left ATL may be more

sensitive on musical attributes.

Impact of ATL on multimodal emotion perception:

Facial Recognition:

In our study, as a whole (Left + Right ATL), there was a marginal improvement in

facial recognition scores between pre-op values and immediate post-op values was

suggestive of significance (p value < 0.10). This improvement persisted into the 3rd

month post-op period where the change was found to be strongly significant


When comparing the change in facial recognition in patients with Left vs. Right

ATL, in our study we found that, in patients undergoing Left ATL, the increase in

facial recognition scores between pre-op and 3rd

month post-op was only

marginally suggestive of significance statistically (p value <0.10). However the

74

increment in the facial recognition scores in patients undergoing Right ATL

between pre-op and 3rd

month post-op was found to be statistically significant

(<0.05).

The findings in our study are unique in the sense that we have reported an increase

in facial recognition after both Left and Right ATL. Previously Dulay et al.9

reported a minor improvement in facial recognition skills in patients with Left

ATL and a decline in facial recognition in patients with Right ATL.

We propose that facial recognition is in part aided by visual memory acumen,

which as our findings suggest is improved after ATL and will be subsequently

reviewed. We postulate that improvement in facial recognition is actually a

reflection of improvement in visual memory, with the proposed mechanism

discussed further on.

Facial Emotion Recognition:

In our study, we found that in patients undergoing both Left ATL and Right ATL,

the change in the facial emotion recognition scores were not found to be

statistically significant.

75

This finding has also been previously reported by Gosselin et al.14

who concluded

that facial emotion interpretation was most probably represented in a multimodal

fashion in both temporal lobes and hence resection of one temporal lobe is unlikely

to significantly affect the ability to decode facial emotions.

Emotion situation recognition:

In our study, we found that in patients undergoing Left ATL, there was an increase

in the emotion situation recognition scores between pre-op and 3rd

month post-op

values which was statistically significant (p value <0.05). The change in the

emotion situation recognition scores in patients undergoing Right ATL was not

found to be statistically significant (p value > 0.10).

These findings are similar to the ones reported by Dulay et al.9 and Gosselin et al.

14

who in their studies had reported a non-specific decline in general emotion

understanding. The findings in our study are unique in that till date no study has

emphasized on the paradigm of recognition of emotional situation. The validity of

this finding in the long term needs to be confirmed by prolonged follow-up of

patients.

76

Repercussions of ATL on memory:

Outcome on Auditory and Verbal Memory:

In our current study, considering both Left and Right ATL as a whole, it was found

that there was a significant improvement in auditory and verbal memory for both

immediate recall and delayed recall modes between pre-op values and 3rd

month

post-op values, which was found to be statistically significant (p value < 0.05). It

was also observed that there was a modest increase in the auditory and verbal

memory scores for both immediate and delayed recall modes between immediate


month post-op values was found to be suggestive of

statistical significance (p value < 0.10).

Verbal outcomes for both Left and Right ATL combined have to interpreted with

caution due to the fact that, Left ATL is traditionally known to negatively affect

verbal memory which may be negated by an improvement in the same by Right

ATL, when both the scores are considered together. In light of this, from our data

we found that ATL in general leads to a significant improvement in verbal

memory.

77

Our findings are in concurrence with those of Lee et al.28

who reported in their

study that there was an overall memory improvement after ATL by about 22%.

Baxendale et al.2

have also reported a modest improvement in memory of around

12% overall in patients undergoing ATL.

On further analysis of verbal memory outcomes in Left ATL vs. Right ATL, our

study revealed that in patients undergoing Left ATL, there was a significant fall of

Auditory and Verbal Memory in the immediate post-op period (p value < 0.05)

which gradually improved and reached almost pre-op baseline levels by the 3rd

month post-op follow-up. In patients undergoing Right ATL, the Auditory and

verbal memory scores improved in the immediate post-op period as well as in the

3rd

month post op both of which were statistically significant (p value < 0.05).

The findings from our study are in agreement with those of Lee et al.28

who

reported in their study that patients with Left ATL had a decline in verbal memory

and patients with Right ATL had a marginal improvement in verbal memory. Even

Sherman et al.48

in their meta-analysis reported a risk to verbal memory with left-

sided temporal surgery occurring in around 44% of patients.

78

Our study differs from previously published reports in that, patients undergoing

Left ATL do indeed have a decline in verbal memory, but our study also found

new evidence that such a decline of verbal memory after Left ATL rapidly

recovers in short term and reaches almost pre-op levels by the 3rd

month. This

finding is more significant in light of the fact that, even though Left ATL carries an

inherent risk of verbal memory deterioration as quoted by prior reports, our study

reveals that such a decline rapidly recovers in the post-op period.

Our study also reveals that patients undergoing Right ATL have a significant

improvement in their verbal memory. This finding again correlates well with

published reports like Baxendale et al.2 who noted in their large study of around

250 patients, of an improvement in verbal memory in patients with Right ATL by

almost around 47%.

Outcome on Visual Memory:

In our study, as a whole (Left ATL + Right ATL), there was an improvement in

visual memory for both immediate recall and delayed recall between pre-op and

immediate post-op period, which was significant statistically (p < 0.05). Also, there

we observed that there was an increase in visual memory scores between pre-op

values and 3rd

month post-op values was found to be strongly significant


79

In our study, when the visual memory outcomes were compared between Left ATL

vs. Right ATL we found that in patients undergoing Left ATL, the visual memory

scores showed an improvement in the immediate post-op period that was

suggestive of significance (p value < 0.10) and this improvement continued well

into the 3rd

month post-op period, at which point of time the increment was

strongly significant statistically (p value < 0.01).

Among patients undergoing Right ATL, the visual memory scores showed an

improvement in the immediate post-op period that was significant statistically (p

value < 0.05). It was also noted that this improvement in visual memory further

improved into the 3rd

month post-op period, at which point of time it attained

strong significance statistically (p value < 0.01).

These findings of our study are similar to those of Sherman et al.48

who reported in

their meta-analysis of improvement in visual memory after Left ATL and transient

decline in visual memory in patients with Right ATL. Lee at al.28

, in their study

have previously reported an improvement of 26% for visual memory in patients

with Left ATL and a decline of 11% in patients with Right ATL.

80

Our study deviates from previously reported studies in literature, in that, we have

found an improvement of visual memory in patients with either Left or Right ATL.

Although the degree of improvement of visual memory is much more acute in

patients with Left ATL, patients with Right ATL also have shown increment in

visual memory scales. This is a new finding in our study in contrast to previously

reported studies wherein there was a reported decline in visual memory in patients

with Right ATL.

Theories abound as to the actual reason for why patients show improvement in

memory functions following ATL. First and foremost, it is generally agreed upon

that the epileptogenic foci or areas are non-functional or more aptly dysfunctional.

It is postulated that the mesial temporal structures undergo functional

reorganization after the onset of seizures, which maybe a predominant mechanism

for the preservation of function in patients with temporal lobe epilepsy. It has also

been found that in patients who show reorganization of memory function to areas

remote to the epileptic foci on f-MRI, the deficits of memory function in the post-

operative period are far fewer.4

81

These observations hint towards the probability that resection of the dysfunctional

neural areas that contribute to the pathogenesis of temporal lobe epilepsy also

indirectly removes the hurdles to memory function.42

It has also been postulated that anatomic localization of memory processing may

play a role in outcome after ATL. Patients showing activation of the ipsilateral

anterior mesial temporal structures during memory encoding tasks are more prone

to have deficits post-operatively, whereas those patients with predominant

posterior hippocampal activation or bilateral mesial temporal activity during

memory encoding are more likely to demonstrate improvement in the

postoperative period.3

Hence overall, from our study it is quite evident that ATL results in neuro-

cognitive changes, both benefit and deficit. Our study evaluated the neuro-

cognitive function at around 3 months postoperatively but the durability of the

findings arrived at is a question that remains unanswered. Our study results

emphasizes the importance of obtaining short term data in order to establish new

cognitive baselines that formulate the follow-up of such patients and also dictate

earlier and more effective interventions that can be put in place for better

rehabilitation of these patients.

82

7. CONCLUSION

The results of this study demonstrate that short-interval follow-up is effective in

elucidating cognitive changes following epilepsy surgery.

In some instances, this lends itself to the identification of patients who could

benefit from early intervention. In other cases, being able to identify the lack of

change, or even cognitive benefit, may influence decisions such as return to work

or school.

Furthermore, the results of this study show that epilepsy surgery is associated with

few cognitive deficits as well as benefits and over a long term epilepsy surgery is

still a safe procedure from the point of view of neuropsychological outcome.

83

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88

MASTER CHART

Case

No. Side

IQ Music

Pitch Rhythm Timbre Loudness

Pre-op

Imm.

Post

Op

3rd

month

post-op

Pre-op

Imm.

Post

Op

3rd

month

post-op

Pre-op

Imm

Post

Op

3rd

month

post-op

Pre-op

Imm

Post

Op

3rd

month

post-op

Pre-op

Imm

Post

Op

3rd

month

post-op

1 Left 82 98 99 14 17 13 15 15 15 13 14 15 19 15 19

2 Left 50 48 58 8 9 12 15 11 14 14 14 13 19 18 19

3 Left 80 92 109 16 18 15 15 15 15 14 14 13 19 19 16

4 Right 67 64 62 12 12 9 15 10 11 13 14 13 19 19 19

5 Right 47 55 48 6 10 10 13 15 13 14 14 14 13 19 19

6 Left 54 15 34 11 8 9 13 12 12 13 12 11 17 12 18

7 Right 92 105 107 10 9 10 15 15 15 15 14 14 19 19 15

8 Left 88 99 108 11 13 12 15 15 14 15 14 13 19 19 19

9 Left 35 42 47 9 9 13 13 15 14 13 13 14 15 15 17

10 Right 42 46 48 11 9 11 13 14 13 10 11 13 17 19 19

11 Left 38 45 42 17 12 13 15 14 14 14 15 14 19 18 19

12 Right 115 129 127 15 15 18 14 15 15 15 15 14 19 19 19

13 Left 52 54 57 11 13 11 18 15 13 14 15 12 19 19 19

14 Right 57 56 56 9 9 12 15 12 15 9 13 14 19 19 19

15 Left 21 29 25 9 11 10 11 11 7 12 11 9 16 15 15

16 Left 54 53 68 13 13 12 15 15 13 15 15 13 19 19 18

17 Left 55 53 50 13 12 9 15 14 13 14 9 14 19 13 19

18 Right 58 69 60 6 12 6 11 13 12 13 14 14 17 15 17

19 Right 67 64 67 8 8 10 14 15 15 15 14 14 19 19 19

20 Right 80 82 92 12 9 8 14 15 15 15 15 15 19 19 19

89

MASTER CHART

Case

No.

Facial Recognition Facial emotion recognition Emotional situation recognition

Pre-op Imm.

Post Op

3rd month

post-op Pre-op

Imm.

Post Op

3rd month

post-op Pre-op

Imm. Post

Op

3rd month

post-op

1 37 36 44 6 6 6 17 20 20

2 35 39 44 4 1 3 20 17 20

3 33 37 40 6 5 6 20 19 20

4 31 30 31 6 5 4 10 18 16

5 34 36 39 4 5 3 20 20 19

6 27 26 27 4 2 3 16 16 19

7 39 39 39 6 6 6 20 20 20

8 34 39 42 6 6 6 20 20 20

9 32 34 35 6 3 5 17 18 17

10 37 33 38 6 6 3 18 19 18

11 27 34 33 6 6 6 19 19 20

12 39 39 40 6 6 6 20 20 20

13 38 35 33 6 6 6 19 17 19

14 25 31 35 4 4 5 18 13 18

15 41 32 36 3 2 2 11 8 13

16 37 40 40 6 6 6 19 20 20

17 28 32 28 4 6 6 17 20 20

18 27 37 34 6 3 6 15 17 20

19 29 39 28 4 6 3 14 16 18

20 41 47 44 6 6 6 20 20 20

90

MASTER CHART

Case

No.

Auditory & verbal

learning AVL IR AVL DR Visual Learning Visual learning IR Visual Learning DR

Pre-op

Imm

Post

Op

3rd

month

post-

op

Pre-op

Imm

Post

Op

3rd

month

post-

op

Pre-op

Imm

Post

Op

3rd

month

post-

op

Pre-

op

Imm

Post

Op

3rd

month

post-

op

Pre-op

Imm

Post

Op

3rd

month

post-

op

Pre-op

Imm

Post

Op

3rd

month

post-

op

1 13 12 15 10 14 14 11 15 15 36 36 36 28 19 28 30 14 28

2 11 8 11 8 2 9 8 9 10 36 34 36 16.5 22 29 16.5 25 28

3 15 13 11 7 10 9 8 14 8 34 36 36 24 30 31 24 30 30

4 10 11 11 6 6 8 7 7 9 32 36 33 6 6 12 4 4 2

5 8 10 13 8 9 13 5 10 10 35 31 36 8 26 19.5 10 22 19.5

6 11 5 7 5 4 7 5 3 4 26.5 12 17 17 9 11.5 14 13 12

7 15 15 15 14 15 15 15 15 15 36 36 36 33 36 36 33 36 36

8 13 9 11 9 10 11 7 9 12 36 36 34 18 21 23 18 18.5 26

9 9 8 12 8 2 8 9 1 9 33 19 30 0 8 20 0 7 16

10 13 15 15 14 15 14 11 14 13 27 29 27.5 13 10 16 14.5 8 15.5

11 10 12 9 8 8 8 9 9 8 34 36 33 15 20.5 27 15 14 25

12 15 15 15 15 14 14 15 14 11 36 36 36 14 18.5 15.5 12.5 18.5 15

13 13 9 10 7 3 6 5 3 9 35 31 32 16 24 23 19 26 24

14 7 10 11 9 8 9 8 7 10 36 36 36 19 24 22 17 24 22

15 13 15 15 14 11 14 14 12 13 30 31 30 14 22 24 19 23 23

16 12 11 14 12 11 13 12 5 13 22 34 36 4.5 15.5 24 4.5 15 20

17 7 4 7 4 3 2 4 1 5 34 34 36 12.5 14.5 28 11 13.5 23

18 10 14 9 7 11 7 7 10 11 33 36 35 17 25 33 17 24 33

19 6 4 8 4 6 3 5 4 3 26 29 36 4 10 9 0 10 7

20 11 14 14 10 11 14 8 8 14 36 34 36 3 19 20 4 20 6.5

91

KEY TO MASTER CHART

Case No. – Case Number

IQ – Intelligence Quotient

Pre-op – Pre-operative score

Imm. Post-op – Immediate post-operative score

3rd

month post-op – 3rd

month post-operative score

AVL – Auditory & Verbal Learning

IR – Immediate Recall

DR – Delayed Recall

95

CONSENT FORM

I___________________________________________ aged _______,

son/daughter of ___________________________________

(Please tick boxes)

•Declare that I have read the above information provide to me regarding

the study: Cognitive effects of anterior temporal lobe resection

and have clarified any doubts that I had. [ ]

• I also understand that my participation in this study is entirely voluntary

and that I am free to withdraw permission to continue to participate at

any time without affecting my usual treatment or my legal rights [ ]

• I understand that my participation in the study will not influence the usual course of my

treatment in the hospital [ ]

• I understand that the study staff and institutional ethics committee

members will not need my permission to look at my health records even if I

withdraw from the trial. I agree to this access [ ]

• I understand that my identity will not be revealed in any information

released to third parties or published [ ]

• I voluntarily agree to take part in this study [ ]

• I received a copy of this signed consent form [ ]

Name: Signature:

Date:

Name of witness:

Relation to participant:

Date:

(Person Obtaining Consent) I attest that the requirements for informed consent for the medical

research project described in this form have been satisfied. I have discussed the research project

with the participant and explained to him or her in nontechnical terms all of the information

contained in this informed consent form, including any risks and adverse reactions that may

reasonably be expected to occur. I further certify that I encouraged the participant to ask

questions and that all questions asked were answered.

______________________________

Name and Signature of Person Obtaining Consent

97

CASE PROFORMA:

Proforma Serial No:

Diagnosis:

Date of Surgery:

Side of Surgery:

Neuropsychological

Test

Pre-

op

Imm

Post-

op

3rd

month

Post-

op

IQ

Pitch Recognition

Rhythm

Recognition

Timbre

Recognition

Loudness

Recognition

Facial Recognition

Facial Emotion

Recognition

Emotion Situation

Recognition

Auditory & Verbal

Learning (IR)

Auditory & Verbal

Learning (DR)

Visual Learning

(IR)

Visual Learning

(DR)

Dr. Sridutt B S October 2016 Department of Neurosurgery...

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