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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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