VISUAL STIMULI ASSOCIATED WITH SWALLOWING ACTIVATE MIRROR...

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CLINICAL DENTISTRY AND RESEARCH 2011; 35(3): 3-16

CorrespondenceYusuke Sanjo, DDS

Department of Oral Medicine, Oral and Maxillofacial Surgery,

Tokyo Dental College,5-11-13, Sugano, Ichikawa-city,

Chiba 272-8513, Japan

Phone: +81 47 3220151

Fax: +81 47 3248577 E-mail: [email protected]

Yusuke Sanjo, DDS Department of Oral Medicine, Oral and Maxillofacial Surgery,

Tokyo Dental College, Chiba, Japan

Yutaka Watanabe, DDS, PhD Department of Oral Medicine, Oral and Maxillofacial Surgery,


Takashi Ushioda, DDSDepartment of Oral Medicine, Oral and Maxillofacial Surgery,


Kazumichi Sato, DDS, PhDOral Cancer Center,


Morio Tonogi, DDS, PhDDepartment of Oral Medicine, Oral and Maxillofacial Surgery,


Shin-ichi Abe, DDS, PhDProfessor, Department of Anatomy,


Gen-yuki Yamane, DDS, PhDProfessor, Department of Oral Medicine,

Oral and Maxillofacial Surgery,

Tokyo Dental College,Chiba, Japan

VISUAL STIMULI ASSOCIATED WITH SWALLOWING ACTIVATE MIRROR NEURONS: AN fMRI STUDY

ABSTRACT

Background and Aim: Human brain research in recent years

has demonstrated the existence of mirror neurons in Brodmann

areas (BA) 44, 6, and BA40. However, there has been almost

no previous research on swallowing and mirror neurons.

We have investigated the activity of mirror neurons during

swallowingrelated visual stimulation.

Subjects and Methods: Subjects were 15 healthy individuals

(6 male, 9 female; average age 27.3 years; right-handed). Brain

activity during the presentation of swallowing movements

was measured using 3T-fMRI. The swallowing movement

videos presented to subjects were conducted using 8 kinds

of stimuli videos, and 8 kind of control videos. fMRI signal

data were acquired based on the blood oxygenation level-

dependent (BOLD) effect to analyze differences between the

various swallowing videos and corresponding control videos by

MATLAB and Simulink Statistical Parametric Mapping 5 (SPM5).

Results: Activity in mirror neuron areas, was observed in

condition of water swallowing, fluoroscopic video, lateral

view (WXL) and chewing and swallowing, fluoroscopic video,

lateral view (CXL). The mirror neuron areas was lefthemisphere

dominant during the presentation of WXL and right-hemisphere

dominant during the presentation of CXL. Significantly stronger

activity was observed during WXL than during CXL.

Conclusion: This study was suggested that activity in the

mirror neuron areas has been observed in research on actual

swallowing. It was suggested that there were dominant

hemisphere like actual swallowing. Numerous studies have

been reported the application of mirror neurons to rehabilitation.

Therefore the use of videos shown in the study may have

applications in swallowing rehabilitation in the future.

Key words: Dysphagia, fMRI, Mirror neuron, Rehabilitation, Swallowing

Submitted for Publication: 10.12.2011

Accepted for Publication : 10.31.2011

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CLINICAL DENTISTRY AND RESEARCH

INTRODUCTION

Dysphagia may result in life-threatening conditions

such as inadequate nutrition, aspiration pneumonia, and

suffocation. Swallowing is a complex function involving

an intricate relationship between numerous muscles and

nerves, and there are currently few scientifically established

rehabilitation methods for its functional recovery.

We have focused on the mirror neuron system in order to

investigate new methods of rehabilitation for such patients.

Mirror neurons are described as neurons that activate in an

individual’s own nervous system as the result of observing

another’s movements, and were discovered in the F5 area of

monkeys’ brains.1-3 They have since also been demonstrated

in the PF area of monkeys’ brains.1, 3

Subsequently, numerous studies have revealed the

existence of mirror neurons in humans in areas corresponding

to those of monkey mirror neurons.1, 3 In addition, research

using the hand mirror neuron system has shown that the

presentation of healthy hand movements is an effective

method of rehabilitating the paralyzed hands of cerebral

infarction patients, suggesting that the presentation of

videos that activate mirror neurons may be effective in the

rehabilitation of motor function.4,5

Some work has already been done on oral movements6-8, but

previous research on mirror neurons and swallowing is the

only work to have suggested the existence of swallowing

mirror neurons.9 In the present study, we increased the

conditions imposed on the videos of swallowing movements

presented, and verified the existence of swallowing mirror

neurons. We also carried out a comparative investigation

of the differences between the left and right hemispheres

and in experimental conditions for the conditions under

which mirror neuron activity was observed. Further, we

investigated the possibility that the mirror neuron activity

seen during this study could be applied to a new method of

rehabilitation for swallowing.

MATERIALS AND METHODS

This study was conducted at the Advanced

Telecommunications Research (ATR) Brain Activity Imaging

Center with the approval of the Ethics Committee of Tokyo

Dental College (Protocol number: 78-A).

Subjects

Subjects were fifteen healthy individuals (age 20–34 years;

average age 27.3 years; 6 males, 9 females). On the day

of the experiment their understanding of the purpose of

the research was verified by means of an explanation in writing, possible risks were explained, and their consent to experimental participation obtained. All were assessed by the Edinburgh Inventory as right-handed.10 They also possessed sufficient visual acuity to perform the tasks.

Study design

The swallowing movement videos presented to subjects were conducted using 8 kinds of stimuli videos: 1) water swallowing, general video, frontal view (WGF); 2) water swallowing, fluoroscopic video, frontal view (WXF); 3) water swallowing, general video, lateral view (WGL); 4) Water swallowing, fluoroscopic video, lateral view (WXL); 5) chewing and swallowing, general video, frontal view (CGF); 6) chewing and swallowing, fluoroscopic video, frontal view (CXF); 7) chewing and swallowing, general video, lateral view (CGL); 8) chewing and swallowing, fluoroscopic video, lateral view (CXL), and 8 kind corresponding control videos consisted of 1000-piece mosaics of 1) - 8) videos; 9) mosaics of WGF; 10) mosaics of WGL; 11) mosaics of WXF; 12) mosaics of WXL; 13) mosaics of CGF; 14) mosaics of CGL; 15) mosaics of CXF; 16) mosaics of CXL. In the previous study, still control images were presented as the control condition.9 However, the possibility existed that they evoked an association with swallowing on the part of the subjects.11 Moreover, compared with the stimulus videos there was almost no movement on the screen, resulting in a difference in the amount of stimulus presented to the subjects, meaning that the appropriateness of these images as controls was questionable. We examined that actual swallowing for a control condition. However, by the preliminary experiment, the brain activity of swallowing that it was difficult to get the result that influence was correct greatly of the noise. Therefore, that way, we would not be able to extract mirror neuron activities with significance. For this reason, in the present study we produced mosaic videos corresponding to each stimulus condition and presented them to the subjects. The mosaic videos made it possible to match the amount of stimulus in the control videos with that of the stimulus videos. Stimulus presentation time was set at 6 seconds for videos of water swallowing condition 1) - 4) and 9) - 12), and 9 seconds for videos of chewing and swallowing condition 5) - 8) and 13) - 16), with a single swallow shown during that time (Figure 1).

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ThE ACTIvITy OF MIrrOr nEurOnS FOr SwAllOwIng STIMulI

A block design was used for the stimulus presentation method, with videos 1) - 16) presented in four separate sessions: A) water swallowing frontal condition: 1), 2), 9), 10); B) water swallowing lateral condition: 3), 4), 11), 12); C) chewing and swallowing frontal condition: 5), 6), 13), 14), and D) chewing and swallowing lateral condition: 7), 8), 15), 16). In sessions A) and B), one block consisted of four consecutive presentations of a single video, after which a 12 seconds blank was inserted between each block, with the presentation of the four different types of video in the order given constituting one cycle. Three cycles were shown in each session. Experiments A) and B) consisted of 432 seconds of presentation in total, and were set to take a total of 144 scans (Figure 2-1).In sessions C) and D), one block consisted of three consecutive presentations of a single video, after which a 12 seconds rest was inserted between each block, with the presentation of the four different types of video in the order given constituting one cycle. Three cycles were shown in each session. Each session lasted 468 seconds, with a total of 156 scans taken (Figure 2-2). All videos were produced in MPEG1 format to enable their control by the presentation

software produced by NeuroBehavioral Systems, which provides precision control of stimulus presentation during fMRI experiments.Intervals of 2 minutes were provided between each session, and the order of presentation of sessions A), B), C), and D) was changed for each subject. This study design applied a previous study.9 Subjects lay supine during fMRI imaging experiments. A Victor DLA-G150CL monitor was used for swallowing videos, and images projected on the screen were displayed via a mirror fixed in place with a cranial coil. The subjects were not given any particular task during the experiment, but were instructed not to move their legs, head, mouth, or tongue while simply observing the visual stimuli. Hitachi Advanced Systems Corp. fMRI high-performance headphones were used to block out sound, and videos were shown with sound inside the fMRI equipment reduced to 20 dBSPL.

Device and imaging conditions

Both T1 and T2-weighted imaging (also called functional imaging or echo planar imaging [EPI]) were carried out with a fMRI instrument (3 Tesla Siemens MAGNETOM Trio, A Tim

Figure 1. Stimuli and corresponding control videos Stimulus presentation time was set at 6.0 s for WGF, WXF, WGL, WXL, and 9.0 s for CGF, CXF, CGL, CXL, with a single swallow shown during that time. These times were the same for the 1000-pieces mosaics videos. All videos were produced in MPEG1 format to enable their control by the presentation software produced by NeuroBehavioral Systems, which provides precision control of stimulus presentation during fMRI experiments. (W: water swallow, C: chewing and swallow, G: general video, X: fluoroscopic video, F: frontal, L: lateral)

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Figure 2-1. Sessions A) and B) In sessions, water swallowing frontal and water swallowing lateral, one block consisted of four consecutive presentations of a single video, after which a 12 s blank was inserted between each block, with the presentation of the four different types of video in the order given constituting one cycle. Three cycles were shown in each session. Experiments A and B consisted of 432 s (approx. 7.2 min) of presentation in total, and were set to take a total of 144 scans.

Figure 2-2. Sessions C) and D) In sessions, chewing and swallowing frontal and chewing and swallowing lateral, one block consisted of three consecutive presentations of a single video, after which a 12 s rest was inserted between each block, with the presentation of the four different types of video in the order given constituting one cycle. Three cycles were shown in each session. Each session lasted 468 s (approx.7.8 min), with a total of 156 scans taken. Intervals of 1-2 min were provided between each sessions.

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system) in the ATR-Brain Activity Imaging Center. The S/N ratio is high for 3T-MRI, enabling high resolution and shorter image acquisition times.12 Imaging was gradient EPI with

the following settings: repetition time (TR), 3 seconds;

Number of slices, 32; matrix size, 64×64 pixels; field of

view (FOV), 192×192 mm; TE, 49 ms; flip angle, 90°; 40

axial slices; plane resolution, 3×3 mm. 40 slices covering the

head were imaged at 123 scans per slice with a voxel size

of 2×2×4 mm and without a slice gap. The first 5 scans in

each session were not used in the analysis because of the

signal value was unstable immediately following the start

of imaging.

Date analysis methods

During these experiments, fMRI measurements were

synchronized with video presentations, and the fMRI signal

was observed on the basis of the blood oxygenation level-

dependent (BOLD) effect to analyze differences between

the various swallowing videos and corresponding control

videos. The “difference method” is a basic experimental

tool for fMRI, and block design is a suitable experimental

method for this. The difference method subtracts brain

activity under control conditions from that under stimulus

conditions, and is an appropriate experimental method for

isolating the brain activity under study.

All images were pre-processed using Statistical Parametric

Mapping 5 (SPM5) software. In SPM5, changes associated

with interactions of brain areas are not considered and,

based on the assumption that each brain area functions

independently, local results are examined statistically

for all pixels. In this study, the head position tended to

move during this long period of imaging. Any slip in head

position was corrected using three-dimensional translation

and rotation in SPM5, with brain imaging data adjusted

three-dimensionally to fit the initial data. Next, data were

normalized in accordance with the standard Montreal

Neurological Institute (MNI) brain. The averaged image was

constructed using the image in the corrected position, and

T2 and T1 structural images were adjusted and normalized

based on this position. Anatomically normalized brain

functional images were smoothed to meet the condition of

a Gaussian random field. Changes associated with activation

generally occur over several pixels and therefore smoothing

makes it easy to detect signal changes due to activation.

Smoothing was conducted using a Gaussian filter (full width

at half maximum (FWHM) = 6×6×8 mm). In this procedure,

signal values and counts are more normally distributed and

can be more effectively used in a statistical model. In fixed effect analysis, signal correlation was calculated using a box-car functional model with a blood flow response function to detect brain area showing statistically significant signal changes due to targeted activation. Furthermore, contrast images were constructed for each subject and a sample t test (a group analysis tool) was performed for these images to detect areas that displayed significant differences sequentially or between sessions. In examining brain activity across the subjects, a sample t test was conducted between brain activity distributions calculated for each subject, and areas with common significant brain activity were identified. As few activated areas were found at p<0.001 without correction of the significance level for multiple comparison, In analyzing the plural data using a random-effects model at p <0.001, z values of activated areas corresponded to 3.09 and higher, and areas showing this value were considered to be activated; these data are summarized (Table 1). The coordinate axes of the results were analyzed using SPM5, expressed as MNI coordinates, and converted into Talairach coordinates using MatLab. The Brodmann area and anatomical position were then estimated from the obtained coordinates in accordance with the Co-Planar Stereotaxic Atlas of the Human Brain (Talairach and Tournoux. 1988). Regions of interest (ROIs) analysis were also done for areas displaying significant activity during presentation of each stimulus. The amount of brain activity was quantified using the regression coefficient for each condition, and calculated it as contrast estimate. Wilcoxon signed rank test was performed that compared under different experimental conditions and between left and right hemispheres.

RESULTS

Brain activity under each condition

Figure 3 shows the MNI standard brain (left and right hemispheres) with brain activity areas obtained from group analysis shown in red. Table 1 shows the Talairach coordinates and Brodmann areas (BA) of brain activity for each condition. The activities for each condition are shown below.

a. Condition of WGF (Figure 3-1, Table1-1)

Activity was observed in BA18 (right hemisphere), regarded as the second visual cortex (V2); BA19 (both hemispheres),

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Figure 3. MNI standard brain with brain activity areas Montreal Neurological Institute (MNI) standard brain (left and right hemispheres) with brain activity areas obtained from group analysis shown in red. A determination of brain activity was made if the significance level of the comparison was p < 0.001 with no multiple comparison correction. (W: water swallow, C: chewing and swallow, G: general video, X: fluoroscopic video, F: frontal, L: rateral)

Brodman areaRight/Left

MNI coordinatesAnatomical position Z value

X Y Z

18 r 46 -80 0 Inferior occipitalis gyrus 3.48

l - - - - -

19 r 64 -72 -8 Middle occipitalis gyrus 4.34

l -54 -68 -4 Middle occipitalis gyrus 3.39

37 r 44 -64 -4 Inferior temporal gyrus 4.08

l -42 -64 2 Inferior temporal gyrus 3.39

Table 1. Talairach coordinates and Z-scores of the activated foci. Montreal Neurological Institute (MNI) coordinates and Brodmann areas (BA) of brain activity and Z value for each condition. A determination of brain activity was made if the significance level of the comparison was p<0.001 with no multiple comparison correction. Table 1-1. Condition of WGF

Table 1-2. Condition of WXF



X Y Z

r - - - - -

l - - - - -

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considered the visual association area (V3); and BA37 (both hemispheres), regarded as the fusiform gyrus.

b. Condition of WXF (Figure 3-2, Table1-2)

No significant activity was observed.

c. Condition of WGL (Figure 3-3, Table1-3)

Activity was observed in BA19 (both hemispheres) and BA37 (left hemisphere).

d. Condition of WXL (Figure 3-4, Table1-4)

As during the presentation of other conditions, activity was observed in BA18 (both hemispheres), 19 (both hemispheres), and BA37 (both hemispheres). In addition, activity was also observed bilaterally in BA44, 45, and BA46 in the frontal lobe; BA6 (both hemispheres), regarded as the premotor area; BA39 (left hemisphere), and BA40 (both hemispheres) in the parietal lobe; and BA7 (both hemispheres), regarded as the somatic sensation association area. This was the greatest amount of activity seen among the stimuli presented in this study.

e. Condition of CGF (Figure 3-5, Table1-5)

Activity was observed bilaterally in BA19 and BA37.

f. Condition of CXF (Figure 3-6, Table1-6)

In addition to BA18, 19, and BA37 (both hemispheres for all), activity was also observed in BA7 (both hemisphere).

g. Condition of CGL (Figure 3-7, Table1-7)

No significant activity was observed.

h. Condition of CXL (Figure 3-8, Table1-8)

As during the presentation of other conditions, bilateral activity was observed in BA18, 19 and BA37. In addition, activity was also observed in BA44 (right hemisphere) and BA45 (right hemisphere) in the frontal lobe and in BA40 (both hemispheres) in the parietal lobe. This was the

second greatest amount of activity seen among the stimuli presented in this study, after WXL. Activity in BA44, 6, or BA40, regarded as mirror neuron areas, was observed in condition of WXL and condition of CXL. Comparison of left and right hemisphere activity in BA44, BA6, and BA40 in condition of WXL (Figure 4)In BA40, significantly stronger activity was observed in the left hemisphere. More activity was observed in the left hemisphere for BA44 and in the right hemisphere for BA6, but these differences were not significant. Comparison of left and right hemisphere activity in BA44, BA6, and BA40 in condition of CXL (Figure 5)In BA44, significantly stronger activity was observed in the right hemisphere. More activity was also observed in the right hemisphere for BA40, but the difference was not significant. No significant activity was observed in BA6. Comparison of amount of activation in each area during condition of WXL and CXL (Figure 6)The amount of activity was significantly greater during WXL in BA44, 6, and BA40, bilaterally.

DISCUSSION

Comparison with other mirror neuron research

A large number of studies based on mirror neurons using, magnetoencephalography (MEG), positron emission tomography (PET), fMRI, and transcranial magnetic stimulation (TMS) has been published, and human mirror neuron areas have been demonstrated.6-9, 13-15 In studies investigating brain activity during the execution and perception of grasping movements by the human hand, and showed that areas BA44 and 40 are activated in both conditions. They emphasize that area BA44 and 6 in particular corresponds to area F5 (including F5c, F5p, and F5a) in monkeys, regarded as the site of mirror neurons.1,3 It

Table 1-3. Condition of WGL

Brodman area

Right/Left


X Y Z



37 r - - - - -


10




X Y Z

40 r 66 -22 26 Inferior parietal lobule 4.23

l -66 -26 28 Inferior parietal lobule 4.72

44 r 48 10 38 Inferior frontal gyrus 4.22

l -52 6 40 Inferior frontal gyrus 3.96



6 r 48 10 50 Middle frontal gyrus 4.72

l -40 0 54 Middle frontal gyrus 4.62

7 r 28 -60 50 Superior parietal lobule 5.20

l -26 -64 54 Superior parietal lobule 4.88

18 r 36 -78 14 Middle occipitalis gyrus 3.34

l -34 -86 14 Middle occipitalis gyrus 5.34



37 r 42 -58 -12 Inferior temporal gyrus 5.19

l -36 -54 -18 Inferior temporal gyrus 5.11

39 r - - - - -

l -34 -72 22 Middle temporal gyrus 5.01

46 r - - - - -


Table 1-4. Condition of WXL



X Y Z



37 r 54 -58 4 Middle temporal gyrus 4.02

l -46 -62 6 Middle temporal gyrus 4.11

Table 1-5. Condition of CGF



X Y Z


l -30 -52 52 Superior parietal lobule 3.78

18 r 34 -84 6 Middle occipitalis gyrus 4.29




37 r 50 -70 2 Inferior temporal gyrus 5.05

l -50 -68 -6 Inferior temporal gyrus 5.20

Table 1-6. Condition of CXF

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X Y Z

r - - - - -

l - - - - -

Table 1-7. Condition of CGL



X Y Z

40 r 30 -38 42 Inferior parietal lobule 4.19

l -44 -38 32 Inferior parietal lobule 4.32


l - - - - -


l - - - - -


l -38 52 58 Superior parietal lobule 3.77

18 r 32 86 6 Middle occipitalis gyrus 3.84




37 r 52 -58 0 Inferior temporal gyrus 5.06


Table 1-8. Condition of CXL

Figure 4. Comparison of left and right hemisphere activity in BA44, BA6, and BA40 of WXL Contrast estimate of left and right hemisphere activity in BA44, 6, and BA40 of WXL, over 15 subjects. Error bars represent standard error of the mean (*p < 0.05) (R: right, L: left)

Contranst estimate

Contranst estimate

R L R L

BA44

Contranst estimate

R L

1.2

1

0.8

0.6

0.4

0.2

0

1.2

1

0.8

0.6

0.4

0.2

0

1.2

1

0.8

0.6

0.4

0.2

0

BA6 BA40

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Figure 5. Comparison of left and right hemisphere activity in BA44, BA6, and BA40 of CXL Contrast estimate of left and right hemisphere activity in BA44 and BA40 of CXL, over 15 subjects. Error bars represent standard error of the mean (**p<0.001)

BA44

Contranst estimate

R L

1.2

1

0.8

0.6

0.4

0.2

0

BA40

Contranst estimate

R L

1.2

1

0.8

0.6

0.4

0.2

0

Figure 6. Comparison of amount of activation in each area during presentation of WXL and CXL Contrast estimate of WXL and CXL activity in BA44, 6, and BA40 of left and right hemisphere, over 15 subjects. Error bars represent standard error of the mean (*p<0.05, **p <0.001) (W: WXL, C: CXL)

BA44(R)

Contranst estimate

W C

1.2

1

0.8

0.6

0.4

0.2

0

BA44(L)

Contranst estimate

1.2

1

0.8

0.6

0.4

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0

BA6(L)

Contranst estimate

1.2

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BA40(L)

Contranst estimate

1.2

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BA6(R)

Contranst estimate

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1

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BA40(R)

Contranst estimate

1.2

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0W C W C

W CW CW C

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has also been reported that area PF in monkeys corresponds

to BA40 in the human. 3,16

In the present study, activity was observed in areas BA44, 6,

and 40 that included the area where activity was suggested

in the previous study, corresponding to the mirror neurons

above, in the two conditions of WXL and CXL. This suggests

the existence of swallowing mirror neurons that were

activated in response to the presentation of swallowing

movement videos. Our previous study, an fMRI investigation

of brain activity during the presentation of auditory and

visual stimuli associated with swallowing, is the only

published research to date on mirror neurons associated

with swallowing, and it suggested the activity of mirror

neurons during the presentation of visual stimuli.9 As there

has been little research on swallowing mirror neurons, at

present it is difficult to make comparisons.

Comparison with brain activity during actual swallowing

A large volume of research has been carried out on

actual swallowing by using fMRI, MEG, and PET, and the

elucidation of brain function during swallowing has been

highly successful.15, 17-20

In a meta-analysis of the results of seven studies on water

swallowing and five on saliva swallowing, involving a total

of 98 subjects, the active areas during water swallowing

were, in descending order of importance: BA4, 43, 44, and

40. During saliva swallowing they were: BA6, 32, 43, and 4.21

These results show that during actual swallowing, activity

was also observed in areas BA44, 6, and 40, which are

regarded as associated with mirror neurons. In light of the

results of the present study, the fact that they are active

during both actual swallowing and the observation of

swallowing suggests the existence of mirror neurons for

swallowing.

Laterality of activation associated with mirror neurons

As shown in Figures 4 and 5, activity in mirror neuron areas

was left-hemisphere dominant during the presentation

of WXL and right-hemisphere dominant during the

presentation of CXL.

According to fMRI research on brain activity during

observation of mouth opening and closing movements, the

right hemisphere was dominant during opening and closing

movements of the mouth in the absence of food, whereas

the left hemisphere was dominant during actual biting and

food-chewing movements.7 Research using MEG to monitor

brain activity during observation of a single movement to

open and close the mouth found that the left hemisphere

was dominant.8 When the results of the present study

are also taken into account, this suggests that the left

hemisphere may be dominant during the presentation of

voluntary movements such as biting food and swallowing

water, whereas the right hemisphere may be dominant

during the presentation of reflex movements such as simple

opening and closing of the mouth or rhythmical chewing.

Research involving actual swallowing has suggested that

the left hemisphere preferentially mediates voluntary

movement during the oral stage, whereas the right

hemisphere mediates reflex movement during the

pharyngeal and subsequent stages.22-24 These findings

suggest that voluntary movements during actual

swallowing are left-hemisphere dominant, whereas reflex

movements are right-hemisphere dominant. The results

of the present study indicate that in the two conditions

in which mirror neuron activity was suggested, the left

hemisphere was dominant during the presentation of

voluntary swallowing in WXL, whereas the right hemisphere

was dominant during the presentation of reflex swallowing

in CXL, demonstrating the same differentiation of function

found in actual swallowing movements. This suggests that

brain function differentiation is involved during both actual

swallowing and its observation.

Comparison of areas of activity associated with mirror

neurons during the presentation of WXL and CXL

As shown in Figure 6, significantly stronger activity was

observed during WXL than during CXL. These two conditions

differed in terms of whether water swallowing or chewing

and swallowing was shown.

During chewing and swallowing, although voluntary

movement is predominant at the start of chewing, the

subsequent rhythmical movement that starts during

chewing is believed to become mainly reflex movement as a

result of automaticity.25 Accordingly, conscious (voluntary)

observation was easier for water swallowing, suggesting

that this also contributed to the increased amount of brain

activity.

Reason for the observation of significant activity in regions

associated with mirror neurons during presentation of the

WXL and CXL conditions

The common factors between the WXL and CXL conditions

under which activity in mirror neuron areas was predominant

were the use of fluoroscopic video and lateral view.

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A comparison of general and fluoroscopic videos showed

that the main feature of general videos was that they

showed the elevation of the larynx. As described above,

however, the feature of fluoroscopic videos is that, unlike

general videos, they enable observers to obtain a large

amount of information by observing muscle and bone

movements. This is because they enable observation of

intra-oral phenomena associated with laryngeal elevation,

from the movement of the hyoid bone to inversion of the

epiglottis, elevation of the soft palate, and movement of

food by the tongue (especially the formation of a bolus by

chewing during chewing and swallowing and its passage

into the pharynx) until it passes through the esophagus. For

this reason, fluoroscopic videos evoked swallowing more

strongly than did general videos, and were suited to the

activation of mirror neuron areas.

A comparison of frontal and lateral views found that in

frontal view images there was a large amount of overlap

in the anatomical information described above between the

oral cavity and the pharynx, particularly under fluoroscopic

video conditions, with bolus movement also perceived as a

simple top-to-bottom movement from the oral cavity to the

esophagus. In lateral view, however, there was no overlap

of the anatomical information described above, and bolus

movement was perceived as an anatomically comprehensible

motion from the oral cavity to the pharynx and esophagus.

Accordingly, as for fluoroscopic videos, lateral views evoked

swallowing more strongly than did frontal views, and were

suited to the activation of mirror neuron areas.

Taking these points into account, the simultaneous

presentation of both factors in the form of fluoroscopic

videos in lateral view evoked a synergistic effect on activity

in mirror neuron areas, suggesting that an interaction effect

was involved.

Application to swallowing rehabilitation

Numerous reports have been published concerning the

application of mirror neurons to rehabilitation. Most

neurorehabilitation techniques rely on methods of inducing

plasticity in the motor cortex.26 Research on hand movement

in patients with long-term sequelae of cerebral infarction

with middle cerebral artery damage has shown that having

patients watch a video of a movement while they undergo

the same movement training increases effectiveness.

Further, the plasticity of the motor cortex has also been

demonstrated, showing that a combination of observation

and movement enables the easier formation of kinesthetic

memories.27-28 Studies of “mirror therapy,” which uses an

actual mirror, have also shown that tricking the vision into

believing that the hand on the paralyzed side is moving

activates movement areas on the damaged side, improving

hand and foot function in stroke patients.4-5 These results

have shown that changes in the plasticity of the motor

cortex and mirror neuron activity are associated with

functional recovery, and further use of the mirror mechanism

is regarded as an important element in promoting functional

recovery.29

Many of these rehabilitation techniques have been reported

for hand movement, for which the existence of mirror

neurons has been proven.4-5

In the hand rehabilitation which applied mirror neuron,

30 minutes of mirror therapy program a day consisting of

wrist and finger flexion and extraction movements or sham

therapy in addition to conventional stroke rehabilitation

program 5 days a week, 2 to 5 hours a day, for 4 weeks.

The effect of this program was shown.4,5 Therefore, it was

thought that observation and execution of swallowing of

30 minutes a day, 5 days a week, for 4 weeks were effective

for swallowing rehabilitation.

Cerebrovascular ascular damage has occurred in many

dysphagia patients, and it is possible that the introduction

of the experimental method described in this study may help

improve swallowing function by employing brain plasticity

resulting from mirror neuron activity. In the present study,

as the greatest mirror neuron activity was observed during

the presentation of WXL, this type of video may be the

most appropriate for activating mirror neurons associated

with swallowing.

The application of mirror therapy to swallowing will require

further investigation to take into account the fact that

effective types of video and stimulus intensity may vary

depending on the location and severity of damage in

patients.

CONCLUSION

In the same way as a previous study, this study suggests

the activity of mirror neurons during the observation of

videos of swallowing movements. The fact that activity

in the same brain areas has been observed in research on

actual swallowing provides indication of the existence of

swallowing mirror neurons. This study suggests that when

swallowing mirror neurons are active, in the same way as

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during actual swallowing, the left hemisphere is dominant

during observation of primarily voluntary movements and

the right hemisphere is dominant during the observation of

primarily reflex movements.

Numerous studies have been reported the application of

mirror neurons to rehabilitation, the use of videos shown in the study may have applications in swallowing rehabilitation in the future.

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