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INTERN TION L
JOURN L OF
PSYCHOPHYSIOLOGY
LS VI R
International Journal of Psychophysiology 22 ( 1996 1-8
Direct electrical stimulation of specific human brain structures
and bilateral electrodermal activity
Constantine A. Mangina *
J. Helen Beuzeron-Mangina
M ontreal Research and Treatment Center and Neurosurgery Deparhnent. M ontreal Neurological Insti tut e, M cGil l Uni versit y, M ontreal,
Quebec, Canada
Received
11
uly 1995; revised 7
February 19%; accepted 13 February 1996
Abstract
We are presenting data of research conducted for the first time with human subjects in whom specific intracerebral sites
were electrically stimulated through intracerebral electrodes with the concomitant recording of bilateral electrodermal
activity. Direct electrical stimulation of specific intracerebral structures for which electrodermal responses
w ere
analyzed
were the amygdalae, the anterior and posterior hippocampi, the anterior cingulate gyri, the frontal cortical convexities and
the mid-region of the second temporal gyri, bilaterally. ANOVA data (side stimulated X stimulation intensity X hand) have
shown that significant main effects were found for side stimulated and stimulation intensity for limbic structures only, These
results provide strong evidence that human bilateral electrodermal activity is under strong ipsilateral control when limbic
structures are stimulated. Moreover, with the stimulation of cortical sites, either absence of response or weak ipsilateral,
contralateral, or bilaterally equal influences seem to be operative
in the elicitation of bilateral electrodermal activity.
Keywords: Electrical brain stimulation; Limbic structure; Cortical site; Hemispheric control; Intracerebral modulator; Bilateral electrodermal
activity; Human
1 Introduction
In psychophysiological research, electrodermal
activity is a valid and reliable electrophysiological
variable of sympathetic nervous system arousal for
investigating various normal and pathological condi-
tions (Roy et al., 1993).
Bilateral electrodermal activity has been used for
the psychophysiological evaluation and the treatment
of learning disabilities (Mangina, 1986, 1989; Mang-
Corresponding author. 3587 University Street Montreal, Que-
bec, Canada, H3A 2B1. Fax: (514) 2841707.
ina and Beuzeron-Mangina, 1988, 1992a,b). In our
previous research, we had identified and standard-
ized bilateral electrodermal parameters of normal
subjects as well as those with learning disabilities.
Moreover, subjects with learning disabilities were
characterized by important bilateral electrodermal
asymmetries which were identified and standardized.
While subjects with an adequate learning potential
maintained the standardized electrodermal activity
bilaterally during cognitive workload, those with
learning disabilities were unable to do so. Conse-
quently, we had devised a psychophysiological treat-
ment methodology for learning disabilities consisting
of a complex procedure during which a variety of
0167-8760/%/ 15.00 0 1996 Elsevier Science B.V. All rights reserved
PII SO167-8760 96)00022-O
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neurophysiologically significant perceptual tasks are
presented by manipulating and maintaining the indi-
vidual’s bilateral electrodermal activation level within
the identified and standardized ‘optimally high’ range
as described elsewhere (Mangina and Beuzeron-
Mangina, 1992a,b). The striking bilateral electroder-
ma1 asymmetries found in children and adolescents
with learning disabilities combined with the applica-
tion of bilateral EDA manipulations during the treat-
ment procedure led us to hypothesize that the psy-
chophysiological treatment procedure was involved
in the manipulation of some neuroanatomical struc-
tures implicated in the modulation of bilateral EDA
which contributed in part to the positive treatment
results.
Very little is known about the hemispheric control
and intracerebral modulators of
human
electrodermal
activity (Boucsein, 1992; Hugdahl, 1984; Miossec et
al., 1985; Roy et al., 1993; Sequeira and Roy, 1993).
Investigations based on brain-lesion data (Luria and
Homskaya, 1963, 1970; Sourek, 1965; Tranel and
Damasio, 1994) and MRI techniques (Raine et al.,
1991; Lencz et al., 1996) provide some useful in&
rect information about certain brain regions that
might be involved in bilateral electrodermal activity.
On the other hand, as compared to these useful
methods, the direct electrical stimulation of specific
human brain structures provides unique possibilities
for investigating the modulators of concomitantly
recorded bilateral electrodermal activity.
No research has ever been conducted in the past
reporting findings of bilateral electrodermal activity
through electrical stimulation of the human brain
(Mangina and Beuzeron-Mangina, 1994). Thus, given
the usefulness of identified and standardized bilateral
electrodermal activity in our procedures, we have
undertaken an investigation pertaining to the hemi-
spheric control and intracerebral representation of
Table I
Electrical stimulation parameters
neural modulators of electrodermal phenomena
(Mangina and Beuzeron-Mangina, 1994).
In this paper, we are reporting data from research
conducted for the first time with human subjects in
whom specific cerebral sites were electrically stimu-
lated through intracerebral electrodes with the con-
comitant recording of bilateral electrodermal activity.
2. Method
2 1 Subjects
Subjects were five young adult surgical patients
(three males and two females, age range 19 to 31
with a mean age 23 years) with intractable epilepsy
with no other brain lesions in whom electrodes were
stereotaxically implanted. Two of the five patients
had epileptic foci suspected to be located in the right
mesio-temporal lobe, another two, in the left mesio-
temporal lobe and one patient in the right frontal
neo-cortex. One week prior and during electrical
stimulation, all five patients were free of anticonvul-
sants and or any other medication. All subjects had
left hemispheric dominance for speech and were
right-handed as evidenced by the Sodium Amytal
Test.
2.2.
Apparatus and procedure
Stereotaxic implantation of depth electrodes was
based on Digital Subtraction Angiography, which
includes Stereoscopic Angiography and Magnetic
Resonance Imaging for anatomical accuracy of elec-
trode placement.
Each electrode was composed of nine recording
contacts. Each contact covered 1 mm* of tissue and
Stimulatig current intensity
Square-wave bipolar stimulation
Bipolar stimulation electrode tip exposure
Stimulating electrode intertip separation
Stimulation duration
Apparatus
0.50-0.75 mAmp
0.5 ms symmetrical pulse duration
1.0 mm*
5mm
4-5s
Nuclear Chicago stimulator
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3
the distance between adjacent recording contacts was
5 mm. The reference electrode was placed in the
skull, without touching the dura, at the level of the
right parieto-occipital junction. The correct position
for each electrode was verified on CT scan. The
EEG was recorded from 32 contacts.
The coverage of frontal lobes was performed by
implanting two arrays of horizontal electrodes with
an orthogonal approach. One electrode was inserted
in the orbital frontal region, passing through the 3rd
frontal gyms in front of the insular vessels and
reaching the mesial surface of the first frontal gyms.
The second electrode passing through the 2nd frontal
gyrus was implanted in the anterior cingulate region.
A lateral orthogonal approach was used for the
stereotaxic coverage of the temporal lobes. Three
depth electrodes were implanted through the second
temporal gyms and inserted horizontally in the
amygdala, the anterior hippocampus and the poste-
rior hippocampus, bilaterally. Table 1 indicates the
direct electrical stimulation parameters used in this
investigation.
For each surgical patient, 48 stimulations were
delivered. This represents a total of 240 stimulations
for all patients combined which were administered
with two different current intensities of 0.50 mAmp
and 0.75 mAmp. Of these 240 stimulations, 120
were delivered with 0.50 mAmp, and another 120
with 0.75 mAmp current intensity. Each site received
two stimulations with 0.50 mAmp and another two
stimulations with 0.75 mAmp current intensity. The
interval between each electrical stimulation was at
least 3 min. All surgical patients had no knowledge
when electrical stimulation was delivered to a spe-
cific intracerebral site.
Direct electrical stimulation of intracerebral struc-
tures for which electrodermal responses were ana-
lyzed were the left and right amygdalae, left and
right anterior and posterior hippocampi, left and right
anterior cingulate gyri, left and right frontal cortical
convexities and left and right mid cortical region of
the second temporal gyri.
Of all 240 stimulations delivered, 70 of them
were rejected from the electrodermal analysis mainly
because of movement artifacts, non-specific electro-
dermal responses prior to brain stimulation and elec-
trical stimulations which triggered epileptic dis-
charge.
Bilateral electrodermal activity (EDA) was
recorded in terms of Skin Conductance Levels (SCLs)
and Skin Conductance Responses (SCRs) by a con-
stant voltage system (0.5 V). Bipolar 1 cm2 Ag/AgCl
disc electrodes in direct contact with the skin were
attached to the index and middle distal phalanges of
both hands. Firm attachment was secured with Mi-
cropore Medical Tape. Prior to attachment of elec-
trodes, skin surface was cleansed with alcohol. Arti-
fact-free and seizure-free bilateral SCRs with an
amplitude higher than 0.05 pmhos and occurring
within 6 s after the onset of electrical stimulation of
specific cerebral sites were statistically analyzed.
2.3.
Statistical analysis
For statistical analysis, a 2 X 2 X 2 ANOVA
comparing side stimulated X stimulation intensity
X hand for each intracerebral site was conducted.
The variable ‘session’ could not be analyzed because
of rejected electrodermal values which occurred ei-
ther within the first or the second stimulation session
of the same intracerebral sites as described earlier.
3. Results
3.1.
Side stimulated
As shown in Table 2, a significant main effect for
side stimulated was found for the amygdalae, the
anterior and posterior hippocampi and the cingulate
gyri. Our data indicate that when the left amygdala,
left posterior hippocampus, left anterior hippocam-
pus and the left cingulate gyms were stimulated, the
amplitude of the left SCRs was significantly higher
than that of the right SCRs. The reverse was found
for the amplitude of the right SCRs when the same
limbic structures in the right side were stimulated.
Thus, these data confirm that ipsilateral excitation of
EDA was present in the hand ipsilateral to the side
electrically stimulated in limbic structures. However,
this main effect was not significant for the left and
right frontal cortical convexities and the mid-region
of the second temporal gyri. This reveals that the
amplitude of SCRs was not different with the stimu-
lation of these cortical regions. Moreover, for these
cortical sites, our results indicate that SCRs were
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Table 2
Direct electrical stimulation of specific intracerebral sites and summary of ANOVA results (side stimulated X stimulation intensity X
hand) for left and right SCRs
Amyg.
aHpc
PHP~
Cing. Fr.Cx.
Mid-T2
Factor (df = 1.4)
F
P
F
P
F
P
F
P F PF P
Side stimulated (SS) 2334.49 O.lE - 05 123.80 0.0003 195.42 0.0001 38.07 0.003 0.662 ns. 0.357 ns.
Stimulation intensity (SD 30.16 0.005 Il.71 0.026 20.5 1 0.01 25.83 0.007 0.878 n.s 7.34 0.053
Hand (LH/RH) 0.193 ns. 2.81 n.s. 0.152 n.s. 3.35 n.s. 3.64 n.s. 0.101 ns.
ss x SI 19.13 0.01 I 11.27 0.028 21.85 0.009 13.07 0.022 0.016 ns. 2.14 ns.
SS X LH/RH 1.99 ns. I 80 ns. 0.321 n.s. 0.531 ns. 0.468 n.s. 0.062 ns.
SI X LH/RH 0.360 n.s. 0.002 n.s. 0.149 ns. 0.042 ns. 0.665 n.s. 0.354 n.s.
Note: Amyg. = amygdalae; aHpc = anterior hippocampi; pHpc = posterior hippocampi; Cing. = cingulate gyri; Fr.Cx. = frontal-cortical
convexities; Mid-T2 = mid-region of the second temporal gyri.
either weak, absent or bilaterally equal as compared
to deep limbic structures.
3 3 Left/ right hand SCR amplitudes
3.2. Stimulation intensity
A significant stimulation intensity main effect was
found for the amygdalae, the anterior and posterior
hippocampi and the cingulate gyri, except for the
frontal cortical convexities and the mid-region of the
second temporal gyri. These data indicate that with
the increase of stimulation intensity in deep limbic
structures, a concomitant increase in the amplitude of
SCRs was obtained (see Table 2).
As for this factor, no significant left and right
hand effect was found. These results imply that when
the left hand SCR amplitudes from the stimulation of
the deep structures of the left side were compared to
the right hand SCR amplitudes obtained from the
stimulation of the deep structures of the right side,
there was no difference in the amplitude between left
and right hand SCRs. The same relationship was
found with the comparison of left and right hand
SCR amplitudes obtained ipsilateral to the side not
stimulated (see Table 2).
Table 3
Direct electrical stimulation of specific intracerebral sites and means and standard deviations of elicited SCRs amplitudes ( pmhos)
Intracerebral Stimulation intensity 0.50 mAmp Stimulation intensity 0.75 mAmp
sites
Left SCR amplitude Right SCR amplitude
Left SCR amplitude Right SCR amplitude
Mean (SD) Mean (SD) Mean (SD) Mean (SD)
L. Amyg. 3.49 (0.41) 0.27 (0. i 8) 4.07 (0.57) 0.39 (0.28)
R. Amyg. 0.26 (0.06) 3.25 (0.38) 0.64 (0.32) 3.84 (0.45)
L. aHpc. 2.59 (0.70) 0.11 (0.05) 3.30 (0.73) 0.14 (0.03)
R. aHpc. 0.07 (0.02) 2.38 (0.82) 0.13 (0.04) 3.05 (0.21)
L. pHpc. 2.65 (0.64) 0.10 (0.06) 3.24 (0.56) 0.12 (0.11)
R. pHpc. 0.09 (0.04) 2.53 (0.61) 0.15 (0.07) 3.14 (0.37)
L. Cing. 2.14 (0.83) 0.04 (0.02) 2.54 (0.70) 0.2 1 (0.27)
R. Cing. 0.05 (0.03) 1.90 (0.77) 0.06 (0.04) 2.40 (0.79)
L. Fr.Cx. 0.84 (0.56) 0.91 (0.42) 0.95 (0.3 1) 0.96 (0.37)
R. Fr.Cx. 0.90 (0.43) 1.020.42) 0.96 (0.38) 0.99 (0.42)
L. Mid-T2 0.04 (0.08) 0.08 (0.11) 0.14 0.08) 0.08 (0.05)
R. Mid-T2 0.06 (0.10) 0.02 (0.04) 0.11 (0.11) 0.18 (0.09)
Note: L. = left;
R. = right; Amyg. = amygdala; aHpc. = anterior hippocampus; pHpc. = posterior hippocampus; Cing. = Cingulate Gyms;
Fr.Cx. = frontal-cortical convexity; Mid-T2 = mid-region of the second temporal gyms.
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A+.
F,.etr Hid-72
LEFT INTRACEREBRAL SITES (.50+.75mA)
Fig. 1. Hierarchy of left hemispheric intracerebral modulators for left SCRs.
3 4 nteractions
Interactions were also examined in this investiga-
tion for all factors. A significant two-way interaction
found was with side stimulated X stimulation inten-
sity for the amygdalae, the anterior and posterior
hippocampi, and the cingulate gyri. That is, the
magnitude of SCRs in deep limbic structures was
dependent upon the interaction of these two factors.
This interaction however, was not significant in cor-
tical structures. No other significant interactions were
found (see Table 2). Means and standard deviations
Phpc
Fr.rn
RIWIT INTF4ii&lEE FlAL 51T~(.50+.75mA)
Fig. 2. Hierarchy of right hemispheric intracerebral modulators for right SCRs.
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of SCR amplitudes elicited by the direct electrical
stimulation of specific cerebral sites with 0.50 and
0.75 mAmp stimulation intensities are indicated in
Table 3.
As illustrated in Figs. 1 and 2, based on data
available from two stimulation sessions for each
level of stimulation intensity combined, we were
able to establish a hierarchy of left and right hemi-
spheric intracerebral modulators for left and right
EDA. For both hemispheres, the amygdala appears
to be first in the hierarchy followed by the posterior
hippocampus, then the anterior hippocampus and the
anterior cingulate gyrus composing the limbic modu-
lators. On the other hand, the frontal cortical convex-
ities were weak contributors and the mid-region of
the second temporal gyri showed a rather very weak
or no contribution as modulators of bilateral EDA.
4. Discussion
The results provide the first direct evidence that
the elicitation of human bilateral EDA is under
strong ipsilateral control when limbic structures are
stimulated. On the other hand, when cortical sites are
stimulated, either absence of response or weak ipsi-
lateral, contralateral, or bilaterally equal influences
seem to be operative in the elicitation of human
bilateral EDA.
Our subjects were anxious, apprehensive and re-
sponsive young adults which might explain the very
high SCRs measured particularly when the amyg-
dalae were electrically stimulated. Moreover, it is
reasonable to assume that the direct electrical stimu-
lation of specific anatomical structures which modu-
late EDA could potentiate SCRs as compared to
other stimuli such as auditory tones or cognitive
tasks. In connection with this, in our investigation,
when the electrical stimulation intensity was in-
creased from 0.50 to 0.75 mAmp, a concomitant
increase in SCR amplitudes was found only for the
limbic structures and in particular for the amygdalae.
This may imply that as compared to cortical sites,
the deep limbic structures have significantly lower
thresholds which in turn may reflect the neuronal
synaptic plasticity which characterizes these limbic
regions (Gloor, 1990). Above-threshold stimulation
of the basolateral part of the amygdaloid nucleus in
lightly anesthetized cats triggered not only phasic but
also tonic EDA (Lang et al., 1964). Amygdalectomy
in monkeys (Bagshaw and Benzies, 1968; Bagshaw
et al., 1965) and in humans (Dallakyan et al., 1970)
attenuated or abolished EDA. An investigation con-
ducted by Tranel and Damasio (1989) however, with
a 60-year-old patient whose both amygdalae were
missing due to herpes simplex encephalitis which he
had developed 12 years ago, suggests that his Skin
Conductance Orienting Responses to stimuli such as
his first name and faces of relatives were normal. In
a latter MRI study of brain-damaged subjects and
SCRs in which the amygdalae and hippocampal for-
mation were not investigated, the same researchers
suggested that amygdala is an important central me-
diator of autonomic activity and that “...the role of
the amygdala remains to be clarified fully” (Tranel
and Damasio, 1994). Our direct brain stimulation
data provide compelling evidence of the modulating
effects of the stimulated amygdalae upon bilateral
EDA in subjects in whom all limbic and other
neuroanatomical structures were present. In fact, our
results established a hierarchy of hemispheric intrac-
erebral modulators for left and right EDA (see Figs.
1 and 2). Stimulation of both amygdalae appear to
yield the highest SCRs in the hierarchy followed by
the other limbic structures. This could be interpreted
by the existence of projections of neuronal circuits
mutually linking the amygdalae with regions of auto-
nomic representation in the hypothalamus and lower
brainstem (Fish et al., 1993; Kapp et al., 1989; Gray,
1989; Price, 1981).
Reviewing all research pertaining to hemispheric
influences on bilateral EDA is beyond the scope of
this paper since such reviews were published by
Hugdahl (1984), Miossec (1985), Boucsein (1992)
and Sequeira and Roy (1993) and in psychosis by
Gruzelier (1979). The overall picture emerging from
these reviews is that task-dependent asymmetries are
interpreted in terms of contralateral inhibition
(Lacroix and Comper, 1979) or by contralateral exci-
tation (Myslobodsky and Rattok, 1975). The diffi-
culty of ascertaining which tasks are ‘purely’ right or
left hemispheric coupled with the lack of any direct
anatomo-physiological evidence casts doubts about
the validity of explanations on the contralateral in-
hibitory or excitatory effects. Studies with brain-
damaged subjects hint towards ipsilateral excitation
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(Luria and Homskaya, 1963; Sourek, 1965) while
Darrow (1937) and Holloway and Parsons (1969)
found increased EDA in the hand contralateral to the
damaged hemisphere.
In our present investigation, the fact that higher
ipsilateral SCRs were obtained when limbic struc-
tures were electrically stimulated should not be sur-
prising since direct pathways connecting the left and
right limbic structures are very limited in humans
and in primates (Amaral et al., 1984; Brazier, 1964;
Lieb et al., 1986, 1987; Pandya and Rosene, 1985;
Wilson et al., 1987). Moreover, the weak and bilater-
ally equal SCRs observed when cortical sites were
stimulated can be explained by the fact that the
neocortical commissural pathways allow the rapid
interhemispheric transfer of activity to contralateral
sites (Lieb et al., 1986, 1987; Wilson et al., 1987).
Nevertheless, even though this interhemispheric
transfer takes place at the neocortical sites, these
same sites remain weak modulators of human SCRs
as our results indicate.
It is worth mentioning that as we descend the
phylogenetic scale, strong functional connections be-
tween the left and right limbic structures of the cat,
rabbit and rat do exist (Andersen, 1959; Hjorth-
Simonsen, 1977; Ramon y Cajal, 1909, 1911) as
opposed to, when ascending the phylogenetic scale
to monkeys and humans (Brazier, 1964; Wilson et
al., 1987). For this reason, researchers who find
bilaterally equal electrodermal responses when stim-
ulating either left or right limbic structures of cats
for example, should not assume that this is also the
case with humans. Our research shows that such an
assumption does not hold true when human intra-
cerebral structures are electrically stimulated. More-
over, as evidenced for the first time in our research,
the direct electrical stimulation of the brain appears
to be the best procedure for the investigation and
understanding of specific hemispheric intracerebral
modulators of human bilateral EDA and it should be
conducted with unanesthetized and unmedicated hu-
man subjects. Nevertheless, in the absence of possi-
bilities to investigate bilateral EDA modulators
through direct electrical stimulation of specific hu-
man brain structures, other indirect techniques such
as MRI correlates, brain-lesion studies as well as
animal preparations could perhaps supplement, ex-
pand and integrate knowledge in this area.
Finally, bilateral EDA appears to be a viable
autonomic indicant of the relative activation of spe-
cific left and right hemispheric human brain struc-
tures. Since bilateral EDA can be continuously ma-
nipulated, monitored and recorded under certain very
rigorously controlled and standardized clinical condi-
tions, it becomes a convenient tool for diagnostic and
treatment purposes. For instance, rigorous manipula-
tion of standardized bilateral EDA has been applied
and has provided one of the important components
of an effective psychophysiological treatment method
for learning disabilities (Mangina and Beuzeron-
Mangina, 1992a,b).
Acknowledgements
The authors wish to express their gratitude to Dr.
Herbert H. Jasper for his helpful comments and
encouragement.
This research was funded in part by the Scientific
Research Grants Foundation of M.R.T.C. for L.A.D.
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