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JOURNAL OF
PSYCHOPHYSIOLOGY
ELSEVIER
A. Mangina
*, J. Helen Beuzeron-Mangina
Montreal Research and Treatment Center and Neurosurgery Deparhnent. Montreal Neurological Institute, McGill University, Montreal,
Quebec, Canada
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
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
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
1-8
0.50-0.75 mAmp
0.5 ms symmetrical pulse duration
1.0 mm*
5mm
4-5s
Nuclear Chicago stimulator
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
Table 2
Direct electrical stimulation of specific
hand) for left and right SCRs
intracerebral
Amyg.
Journal
of ANOVA
PHP~
X stimulation
Fr.Cx.
PF
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.
pHpc = posterior
gyri.
equal as compared
intensity
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
deviations
Stimulation
( pmhos)
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.
Cing. = cingulate
Mid-T2
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;
F,.etr
A+.
LEFT INTRACEREBRAL
Hid-72
SITES (.50+.75mA)
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)
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
CA. Mangina,
J.H. Beuzeron-Mangina/lnternational
I-8
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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