INTERNATIONAL

JOURNAL OF
PSYCHOPHYSIOLOGY

ELSEVIER

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

Montreal Research and Treatment Center and Neurosurgery Deparhnent. Montreal Neurological Institute, McGill University, Montreal,
Quebec, Canada

Received 11July 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 were 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;
activity; Human

Limbic structure; Cortical site; Hemispheric

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 conditions (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,
bec, Canada, H3A 2B1. Fax: (514) 2841707.
l

Que-

0167-8760/%/$15.00
0 1996 Elsevier Science B.V. All rights reserved
PII SO167-8760(96)00022-O

control; Intracerebral

modulator;

Bilateral electrodermal

ina and Beuzeron-Mangina,

1988, 1992a,b). In our
previous research, we had identified and standardized 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. Consequently, we had devised a psychophysiological
treatment methodology for learning disabilities consisting
of a complex procedure during which a variety of

CA. Mangina,

J.H. Beuzeron-Mangina/International

neurophysiologically
significant perceptual tasks are
presented by manipulating
and maintaining the individuals bilateral electrodermal activation level within
the identified and standardized optimally high range
as described elsewhere (Mangina
and BeuzeronMangina, 1992a,b). The striking bilateral electroderma1 asymmetries found in children and adolescents
with learning disabilities combined with the application of bilateral EDA manipulations
during the treatment procedure led us to hypothesize that the psychophysiological
treatment procedure was involved
in the manipulation
of some neuroanatomical
structures 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 hemispheric control and intracerebral
representation
of

Table I
Electrical

stimulation

Journal

of Psychophysiology

22 (1996)

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 stimulated through intracerebral electrodes with the concomitant 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 mesiotemporal lobe and one patient in the right frontal
neo-cortex.
One week prior and during electrical
stimulation, all five patients were free of anticonvulsants 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 electrode placement.
Each electrode was composed of nine recording
contacts. Each contact covered 1 mm* of tissue and

parameters

Stimulatig current intensity

Square-wave bipolar stimulation
Bipolar stimulation electrode tip exposure
Stimulating electrode intertip separation
Stimulation duration
Apparatus

1-8

0.50-0.75 mAmp
0.5 ms symmetrical pulse duration
1.0 mm*
5mm
4-5s
Nuclear Chicago stimulator

CA. Mangina, J.H. Beuzeron-Mangina /International Journal of Psychophysiology 22 (1996) 1-8

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 posterior 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 specific intracerebral site.
Direct electrical stimulation of intracerebral structures for which electrodermal responses were analyzed 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 electrodermal responses prior to brain stimulation and electrical stimulations which triggered epileptic discharge.

Bilateral electrodermal
activity (EDA) was
recorded in terms of Skin Conductance Levels (SCLs)
and Skin Conductance Responses (SCRs) by a constant 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 Micropore Medical Tape. Prior to attachment of electrodes, skin surface was cleansed with alcohol. Artifact-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 either 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 hippocampus 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 stimulation of these cortical regions. Moreover, for these
cortical sites, our results indicate that SCRs were

CA. Mangina, J.H. Beuzerun-Mangina /Intemutional

Table 2
Direct electrical stimulation of specific
hand) for left and right SCRs

intracerebral

sites and summary

aHpc

Amyg.

Journal

r?fPsychophysiology 22 (1996) 1-8

of ANOVA

results (side stimulated

Cing.

PHP~

X stimulation

Fr.Cx.

PF

Side stimulated (SS)

Stimulation intensity (SD
Hand (LH/RH)
ss x SI
SS X LH/RH
SI X LH/RH

2334.49
30.16
0.193
19.13
1.99
0.360

O.lE - 05
0.005
ns.
0.01 I
ns.
n.s.

123.80
Il.71
2.81
11.27
I .80
0.002

0.0003
0.026
n.s.
0.028
ns.
n.s.

195.42
20.5 1
0.152
21.85
0.321
0.149

0.0001
0.01
n.s.
0.009
n.s.
ns.

38.07
25.83
3.35
13.07
0.531
0.042

0.003
0.007
n.s.
0.022
ns.
ns.

0.662
0.878
3.64
0.016
0.468
0.665

ns.
n.s
n.s.
ns.
n.s.
n.s.

either weak, absent or bilaterally

to deep limbic structures.
3.2. Stimulation

pHpc = posterior
gyri.

equal as compared

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).

Table 3
Direct electrical
Intracerebral
sites

L.
R.
L.
R.
L.
R.
L.
R.
L.
R.
L.
R.

Amyg.
Amyg.
aHpc.
aHpc.
pHpc.
pHpc.
Cing.
Cing.
Fr.Cx.
Fr.Cx.
Mid-T2
Mid-T2

stimulation

of specific intracerebral

Stimulation

hippocampi;

3.3. Left/

P
0.357
7.34
0.101
2.14
0.062
0.354

gyri; Fr.Cx. = frontal-cortical

right hand SCR amplitudes

deviations

Stimulation

of elicited SCRs amplitudes

( pmhos)

intensity 0.75 mAmp

Left SCR amplitude

Mean (SD)

Right SCR amplitude

Mean (SD)

Left SCR amplitude

Mean (SD)

Right SCR amplitude

Mean (SD)

3.49
0.26
2.59
0.07
2.65
0.09
2.14
0.05
0.84
0.90
0.04
0.06

0.27
3.25
0.11
2.38
0.10
2.53
0.04
1.90
0.91

(0. i 8)
(0.38)
(0.05)
(0.82)
(0.06)
(0.61)
(0.02)
(0.77)
(0.42)
1.02(0.42)
0.08 (0.11)
0.02 (0.04)

4.07
0.64
3.30
0.13
3.24
0.15
2.54
0.06
0.95
0.96

0.39 (0.28)
3.84 (0.45)
0.14 (0.03)
3.05 (0.21)
0.12 (0.11)
3.14 (0.37)
0.2 1 (0.27)
2.40 (0.79)
0.96 (0.37)
0.99 (0.42)
0.08 (0.05)
0.18 (0.09)

(0.41)
(0.06)
(0.70)
(0.02)
(0.64)
(0.04)
(0.83)
(0.03)
(0.56)
(0.43)
(0.08)
(0.10)

ns.
0.053
ns.
ns.
ns.
n.s.

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).

sites and means and standard

intensity 0.50 mAmp

Cing. = cingulate

Mid-T2

Factor (df = 1.4)

Note: Amyg. = amygdalae;

aHpc = anterior hippocampi;
convexities; Mid-T2 = mid-region of the second temporal

intensity

(0.57)
(0.32)
(0.73)
(0.04)
(0.56)
(0.07)
(0.70)
(0.04)
(0.3 1)
(0.38)
0.14(0.08)
0.11 (0.11)

Note: L. = left; R. = right; Amyg. = amygdala; aHpc. = anterior hippocampus; pHpc. = posterior
Fr.Cx. = frontal-cortical
convexity; Mid-T2 = mid-region of the second temporal gyms.

hippocampus;

Cing. = Cingulate

Gyms;

CA. Mangina. J.H. Beuzeron-Manginu /International JOWM~ ofPsychophysiology 22 (1996) 1-8

F,.etr

A+.

LEFT INTRACEREBRAL

Hid-72

SITES (.50+.75mA)

Fig. 1. Hierarchy of left hemispheric intracerebral modulators for left SCRs.

3.4.Interactions

Interactions were also examined in this investigation for all factors. A significant two-way interaction
found was with side stimulated X stimulation intensity 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 cortical structures. No other significant interactions were
found (see Table 2). Means and standard deviations

Fr.rn

Phpc

RIWIT

INTF4ii&lEE#FlAL

51T~(.50+.75mA)

Fig. 2. Hierarchy of right hemispheric intracerebral modulators for right SCRs.

CA Mangina, J.H. Beureron-Manginn /International Journal of Psychophysiology 22 (1996) 1-8

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 hemispheric 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 modulators. On the other hand, the frontal cortical convexities 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 ipsilateral, contralateral,
or bilaterally equal influences
seem to be operative in the elicitation of human
bilateral EDA.
Our subjects were anxious, apprehensive and responsive young adults which might explain the very
high SCRs measured particularly when the amygdalae were electrically stimulated. Moreover, it is
reasonable to assume that the direct electrical stimulation of specific anatomical structures which modulate 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 increased 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 conducted 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 formation were not investigated, the same researchers
suggested that amygdala is an important central mediator 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 intracerebral 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 autonomic 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 excitation (Myslobodsky
and Rattok, 1975). The difficulty 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 inhibitory or excitatory effects. Studies with braindamaged subjects hint towards ipsilateral excitation

CA. Mangina,

J.H. Beuzeron-Mangina/lnternational

(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 structures were electrically stimulated should not be surprising 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 bilaterally 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 between the left and right limbic structures of the cat,
rabbit and rat do exist (Andersen,
1959; HjorthSimonsen,
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 stimulating 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 intracerebral structures are electrically stimulated. Moreover, 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 human subjects. Nevertheless, in the absence of possibilities to investigate
bilateral
EDA modulators
through direct electrical stimulation of specific human brain structures, other indirect techniques such
as MRI correlates, brain-lesion
studies as well as
animal preparations could perhaps supplement,
expand and integrate knowledge in this area.

Journal of Psychophysiology 22 (1996)

I-8

Finally, bilateral EDA appears to be a viable

autonomic indicant of the relative activation of specific left and right hemispheric human brain structures. Since bilateral EDA can be continuously
manipulated, monitored and recorded under certain very
rigorously controlled and standardized clinical conditions, it becomes a convenient tool for diagnostic and
treatment purposes. For instance, rigorous manipulation 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 BeuzeronMangina, 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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