Physiology and Behavior, Vol. 12, pp. 913-918. Brain Research Publications Inc., 1974. Printed in the U.SoA.

Caudate Nucleus Stimulation Impairs

the Processes of Perceptual Integration'
J. G R I N B E R G - Z Y L B E R B A U M , M. B. C A R R A N Z A , G. V. C E P E D A , T. C. V A L E
A N D N. N. S T E I N B E R G

Psychophysiological Research Laboratory, Psychology College, Universidad An~huac,

Apdo. Postal 10-844, M~xico 1 O, D. F. M~xico

(Received 22 N o v e m b e r 1973)

GRINBERG-ZYLBERBAUM, J., M. B. CARRANZA, G. V. CEPEDA, T. C. VALE AND N. N. STEINBERG. Caudate

nucleus stimulation impairs the processes of perceptual integration. PHYSIOL. BEHAV. 12(6) 913-918, 1974. - Single
brief electrical pulses delivered to the caudate-putamen complex of rats while they are watching the performance of trained
rats in a Skinner type box, prevent the acquisition of the observed instrumental behavior. Intact rats or nonstimulated
implanted rats showed a perfect acquisition of the observed instrumental behavior.

Caudate-putamen complex Electrical stimulation Learning by observation

E X P E R I M E N T A L evidence indicates that single electrical
pulses of very short duration applied to the caudate nucleus
interfere with the learning processes [ 15, 22, 29, 3 0 ] , while
similar stimulation o f adjacent structures like the corpus
callosum, the internal capsule or the white m a t t e r adjacent
to the cerebral cortex does not [ 2 9 ] . On the o t h e r hand,
lesions o f the caudate nucleus [28] or the t e m p o r a r y
blockade o f its electrical activity by the topical application
of local anesthetics [3] or KC1 3M [ 2 5 ] prevent the
learning of different t y p e s o f paradigms, such as classic
conditioning [ 25 ], active avoidance [ 18 ], passive avoidance
[ 1 2 ] , a p p r o x i m a t i o n [241, c o n d i t i o n e d inhibition [ 4 ] ,
delay conditioning [7] and instrumental (Skinner type)
conditioning [ 24 ].
Even though the above evidence points toward a
normally functioning caudate nucleus as a requisite for the
learning process to take place, it is difficult to decide
whether the disturbances, attending damage o f the caudate
nucleus should be attributed to a m o t o r deficit, which
prevents the animals to display the learned behavior or
rather if they are due to inability to integrate and store the
perceptual i n f o r m a t i o n associated with the learning process.
Demetrescu [8, 9, 10] and K r a u t h a m e r [19] have
postulated that the caudate nucleus participates in the
sensory processes through its inhibitory influence u p o n
those structures involved in the transmission of the afferent
information.
The above m e n t i o n e d data suggest that the role o f the
caudate nucleus in the learning processes might be related
to the integration of the perceptual information necessary
for the acquisition o f new behaviors. By integration we
mean: c o d i f i c a t i o n of information, comparison with
previously codified data and subsequent storage of the
c o m p a r e d codified i n f o r m a t i o n in memory.
The following experiments were intended to test the
preceding postulation.
EXPERIMENT l
Me th od
First, it was necessary to design a special technique that
would conclusively separate the integration of the percep-
tual i n f o r m a t i o n from the m o t o r processes.
This included a learning paradigm allowing a rat to
observe another rat while the latter was performing a
previously learned task and a test to find out if this observa-
tion period p e r m i t t e d the first rat to acquire the same
behavior.
Ten naive, male, albino rats, 3 to 4 m o n t h s old, reared
under the same conditions in the animal colony of the
Universidad An~huac, were used. These animals were
trained in a Skinner box during 4 consecutive sessions of
10 rain each (association sessions) to drink water from an
a u t o m a t i c device, which made a noise when it was activa-

1The authors express their gratitude to Prof. Or. Alberto Guevara Rojas for his critical analysis of the manuscript, Miss Libe Broid for her
help in it's redaction and Miss Laura Verduzco for her technical assistance.

913
 914 G R I N B E R G - Z Y L B E R B A U M E T AL.

FIG. 1. Device used in the experiment. One implanted rat watches the interior of a Skinner box in which a trained rat is pressing a lever in
order to obtain water as a reward. The cables connected to the implanted rat are used to stimulate her caudate-putamen complex during the
observation sessions.

ted. Before every session, the rats o f all described groups Results
were deprived o f water during 24 hr. E x c e p t for this period,
During the test sessions, the rats of Group A e x h i b i t e d a
water and f o o d were available ad lib.
clear lever pressing behavior when i n t r o d u c e d into the
After these association sessions, the rats were r a n d o m l y
Skinner box which persisted during 15 rain of the first
separated into t w o groups o f 5 rats each. Those o f the first
session and increased clearly during the second session,
group (A) were placed within a t r a n s p a r e n t lucite box
48 hr after the first one. On the contrary, the rats of Group
(shown in Fig. 1) from which they could observe during
B only by chance pressed the lever during the first test
15 min (observation sessions) the interior of the Skinner
session.
box in which a rat pressed a lever in order to obtain water
The differences in the n u m b e r o f lever pressings o f b o t h
from the same a u t o m a t i c drinking device which the
groups during the first and the second test sessions are
observer had used during the previous association sessions.
The observation sessions were r e p e a t e d every o t h e r day d e p i c t e d in Fig. 2. These differences were statistically sig-
until a total o f 5 were c o m p l e t e d . Forty-eight hr after the nificant at p<0.01 ( S t u d e n t t 9.6) [ 2 0 ] .
This result indicates that under these c o n d i t i o n s it is
fifth o b s e r v a t i o n session the rats were i n t r o d u c e d into the
enough for a rat to observe the manifestation o f learning o f
Skinner box and the n u m b e r o f lever pressings during
a n o t h e r rat to acquire it.
15 min was recorded (test sessions).
Once that the above had been d e m o n s t r a t e d , this tech-
The s e c o n d group (B) was s u b m i t t e d to exactly the same
nique was used to test the participation of the caudate-
t r e a t m e n t as Group A, e x c e p t that during the observation
p u t a m e n c o m p l e x in learning by observation, as follows.
sessions, a rat not trained to press the lever was placed into
the Skinner box.
EXPI.IRIMENT 2
During the test session the e x p e r i m e n t e r only placed the
rat i n t o the Skinner b o x , and t h e n limited himself to n o t e
Method
the behavior o f the animals, which received water as
r e i n f o r c e m e n t for pressing the lever; the lever was cleaned F o u r t e e n male albino rats 3 to 4 m o n t h s old, reared as
at the end o f each rat's session. described, were p e r m a n e n t l y i m p l a n t e d with stainless steel
CAUDATE NUCLEUS AND PERCEPTUAL INTEGRATION
150-
INTACT RATS
F-1GROUP A
1 GROUP B
tO0.
! [18].
!,o
m
1 2 I 2 TEST SESSION
FIG. 2. The white bars represent the average of lever pressing made
during the first (l) and the second (2) test sessions by the intact
group of rats (A); these animals observed the behavior of a well
trained rat located in the interior of a Skinner box. The black bars
represent the same thing for the group of rats (B) that observed the
behavior of a non trained animal located in the interior of the same
Skinner box. We found statistically significant differences (p<0.01)
between the two groups. This result indicates that learning by
observation exists in the rat.
bipolar concentric electrodes in b o t h c a u d a t e - p u t a m e n
complexes according to the following coordinates: lateral,
3 m m from the midline; height, 4.5 m m from the dura
mater; anterior on the bregma line, with the rat horizon-
tally placed.
Seven days after the operation, all the rats were submit-
ted to the procedure already described for the rats of
Group A ( E x p e r i m e n t 1). After 4 water-drinking associa-
tion sessions, the rats were separated at r a n d o m in two
groups (C and D) and submitted to 5 observation sessions,
during which the rats of group C were stimulated through
the electrodes implanted in b o t h caudate-putamen com-
plexes with single square pulses of 0.5 msec duration and
500 uA o f intensity, every 10 sec during the 15 rain of the
observation s e s s i o n s (Fig. 1). The stimulation was
p e r f o r m e d with a Grass $48 stimulator, coupled to a Grass
isolation unit and to a constant current Grass unit.
The rats o f Group D were also c o n n e c t e d to the stim-
ulator but did not receive any electrical pulses.
At the end o f the experiments, the animals were deeply
anesthetized and their brains were perfused with a 10%
Formalin solution injected in the left ventricle of the heart,
preceded by 50 ml of a 0.9% saline solution. The brains
were maintained during one week in a 10% F o r m a l i n
solution after which transversal frozen section, 50 microns
thick, were made. The histological sections were used as
negatives to make photographic prints and the location of
the electrodes were established with the help o f a stereo-
taxic atlas [ 14,23].
915
Results
During the test sessions, the rats of the previously
stimulated group (C) only pressed the lever by chance, while
the rats of the non-stimulated group (D) showed a clear
lever pressing behavior. The above results are depicted in
Fig. 3, in which the differences in the average of pressing
for the t w o implanted groups during the first and the
second test sessions can be seen. These differences are
statistically significant with a p < 0 . 0 2 (Student t 2.99)
15o.
IMPLANTED RATS
~125. ["-] GROUPO
1 GROUP C
100.
g0-
25-
1 2 t 2 TEST SESSION
FIG. 3. The white bars represent the average of lever pressings made
during the first (I) and the second (2) test sessions by the implanted
but not stimulated group of rats (D). The black bars represent the
same thing for the implanted and stimulated group of rats (C). We
found statistically significant differences-(p<0.02) between the two
groups. This result indicates that stimulation of the caudate-
putamen complex interferes with the learning by observation in rats.
It is to be noted that no statistically significant differ-
ences in the instrumental behavior of Groups A and D were
found, which means that neither the surgical procedure nor
the chronic implantation affect the learning by observation.
Similarly no differences were found between Groups B and
C, showing that the electrical stimulation of the caudate-
putamen c o m p l e x interferes with the learning by observa-
tion.
The histological analysis o f the implanted rats showed
that, without exception, the electrodes were in the medial
portion of the caudate-putamen c o m p l e x (Fig. 4).
GENERAL DISCUSSION
The results obtained in E x p e r i m e n t 1 indicate that
learning by observation takes place in the rat, as was shown
before by other authors [6,17] in the cat and the rhesus
monkey.
We did not notice any significant m o v e m e n t s displayed
by the rats during the observation sessions, this means that
in order to acquire an observed instrumental learning
paradigm overt m o t o r behavior is not necessary.
916
GROUP C
GROUP D
FIG. 4. The histological analysis of the implanted rats showed that, in the rats of both groups,
without exception, the electrodes were located in the medial portion of the caudate-putamen
complex.
The only way to explain this result is to p o s t u l a t e t h a t
the brain o f the rat is capable of p e r f o r m i n g very c o m p l e x
associations b e t w e e n codified a f f e r e n t i n f o r m a t i o n trans-
m i t t e d by way of one or more sensory channels.
The i n f o r m a t i o n available to o u r animals d u r i n g the
o b s e r v a t i o n sessions was, in the first place, the behavioral
m a n i f e s t a t i o n displayed b y the trained rat. This b e h a v i o r
consisted of a c o m p l e x s e q u e n c e of m o v e m e n t s associated
with pressing the lever, t u r n i n g the b o d y towards the drink-
ing place and finally d r i n k i n g the water. In the second
place, the s o u n d made by the a u t o m a t i c d r i n k i n g device
w h e n t h e lever was activated, and finally, the internal
i n f o r m a t i o n related to the thirst of the observer rat.
We t h i n k t h a t all this i n f o r m a t i o n (except the lever
pressing) was in some sense familiar for the observer rat,
because of the previous t r a i n i n g (association sessions) t h a t
he had. Learning by o b s e r v a t i o n possibly consisted in
storing i n t o the already familiar sequence the c o d i f i c a t i o n
of t h e viewed lever pressing behavior.
G R I N B E R G - Z Y L B E R B A U M E T AL.
The p a r t i c i p a t i o n of the c a u d a t e nucleus in the integra-
tion of the f o r m e r processes was d e m o n s t r a t e d in Experi-
m e n t 2 in which the electrical s t i m u l a t i o n of this s t r u c t u r e
d u r i n g the o b s e r v a t i o n sessions impaired the a c q u i s i t i o n of
the observed i n s t r u m e n t a l behavior.
T w o questions are i m m e d i a t e l y raised by this d e m o n -
s t r a t i o n : (1) what are the n e u r o p h y s i o l o g i c a l effects of
s t i m u l a t i n g the c a u d a t e nucleus and (2) what is the relation
b e t w e e n these effects and the i n t e g r a t i o n of the a f f e r e n t
i n f o r m a t i o n ? One possible answer to the above q u e s t i o n s is
t h a t s t i m u l a t i o n o f the c a u d a t e nucleus interferes w i t h the
p e r c e p t u a l processes t h r o u g h its i n h i b i t o r y i n f l u e n c e u p o n
t h o s e s t r u c t u r e s involved in the analysis and i n t e g r a t i o n of
the a f f e r e n t i n f o r m a t i o n .
This view is in accord with the evidence p r e s e n t e d by
D e m e t r e s c u [8, 9, 10], K r a u t h a m e r [19] and B u c h w a l d
[ 5 ] , and with P r i b a m ' s analysis [ 2 6 ] . In this sense, stimu-
lation of the c a u d a t e nucleus in o u r e x p e r i m e n t , only
activated the i n h i b i t o r y o u t f l o w f r o m this s t r u c t u r e , block-
CAUDATE NUCLEUS AND PERCEPTUAL INTEGRATION
ing b y its a c t i o n t h e t r a n s m i s s i o n a n d i n t e g r a t i o n o f t h e
a f f e r e n t i n f o r m a t i o n in t h e s t r u c t u r e s related w i t h these
processes.
A l t h o u g h this possibility is admissible, we t h i n k t h a t o u r
results can be best e x p l a i n e d if we take i n t o a c c o u n t t h e
following c o n s i d e r a t i o n s :
(1) T h e stimuli t h a t activate in o p t i m a l f o r m t h e n e u r o n s
o f t h e visual s y s t e m are relatively simple at t h e level of t h e
ganglionic cells o f t h e r e t i n a a n d b e c o m e m o r e c o m p l e x at
the cortical level.
At t h e same time, t h e visual fields increase in size
[ 1 1 , 1 6 ] . These facts can be e x p l a i n e d if we assume high
c o n v e r g e n c e p a t t e r n s o f c o n n e c t i o n s as we m o v e away f r o m
t h e p e r i p h e r y o f t h e visual system.
High c o n v e r g e n c e p a t t e r n s of c o n n e c t i o n s reduce t h e
n u m b e r o f physical c h a n n e l s necessary t o t r a n s m i t i n f o r m a -
t i o n w i t h a c o r r e s p o n d i n g increase in the c o m p l e x i t y o f t h e
signals t h a t each one of t h e m conveys.
(2) T h e c a u d a t e n u c l e u s is a polisensorial s t r u c t u r e [ I, 13 ]
its n e u r o n s r e s p o n d to d i f f e r e n t k i n d s o f a f f e r e n t i n f o r m a -
tion, i n c l u d i n g t h o s e t r a n s m i t t e d t h r o u g h t h e visual s y s t e m
[ 2 , 2 7 ] . This visual i n f o r m a t i o n is possibly related w i t h the
activity o f the i n f e r o t e m p o r a l c o r t e x [26] or t h e occipital
c o r t e x [ 5 ].
If t h e high c o n v e r g e n c e p a t t e r n s o f c o n n e c t i o n s are
m a i n t a i n e d at t h e level o f t h e c a u d a t e nucleus, its n e u r o n s
w o u l d receive highly c o m p l e x and previously i n t e g r a t e d
i n f o r m a t i o n of various modalities, t h u s a c o m p a r i s o n
b e t w e e n t h e arriving c o m p l e x signal b e c o m e possible at this
level. On t h e o t h e r h a n d , t h e n o r m a l activity o f t h e c a u d a t e
n u c l e u s seems i n d i s p e n s a b l e for t h e a c q u i s i t i o n a n d reten-
t i o n o f learned i n f o r m a t i o n [3, 4, 7, 12, 15, 18, 22, 24, 25,
28, 29, 3 0 ] , this evidence i n d i c a t e s t h a t c a u d a t e n u c l e u s
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a f f e r e n t i n f o r m a t i o n b u t possibly also in the association
a n d storage o f the resulting c o m p a r i s o n s . We t h i n k t h a t
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n o t occur.
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these c o m p a r i s o n and storage processes.
Morrell [21] has p r e s e n t e d evidence a b o u t t h e existence
o f polisensorial n e u r o n s t h a t can c h a n g e t h e i r p a t t e r n s o f
response w h e n t w o stimuli are s i m u l t a n e o u s l y p r e s e n t e d ,
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o n e o f t h e stimuli is given.
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d e p e n d i n g o n t h e s e q u e n c e and c o m p l e x i t y o f arriving
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plus i n f o r m a t i o n a b o u t t h e i n t e r n a l state of the animal.
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918
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