Neurobiology of Learning and Memory 72, 13–27 (1999)

Article ID nlme.1998.3899, available online at http://www.idealibrary.com on

Inferior Olive Lesions Impair Concurrent Taste

Aversion Learning in Rats
C. Mediavilla, F. Molina, and A. Puerto
Psychobiology Area, University of Granada, Granada, Spain

Taste aversion learning can be established according to two different procedures,

concurrent and sequential. For the concurrent task, two different taste stimuli are
offered at the same time, one associated with simultaneous intragastric administration
of an aversive stimulus and the other associated with physiological saline. This dis-
crimination is learned by sham-lesioned control animals and by animals with lesions in
the cerebellar cortex but not by rats lesioned in the inferior olive. At the same time,
animals with lesions in the inferior olive and sham-lesioned animals achieve sequential
learning when the gustatory stimuli are offered individually during each daily session.
The results obtained show that electrolytic lesions in the inferior olive impair acquisi-
tion of concurrent learning and are analyzed in terms of an anatomical system consist-
ing of the vagus nerve, inferior olive, and cerebellum, which differentiates between the
two modalities of taste aversion learning, concurrent and sequential. © 1999 Academic Press
Key Words: inferior olive; cerebellar cortex; taste aversion learning; concurrent
learning.

INTRODUCTION

Taste aversion learning (TAL) occurs when a specific type of food or gusta-
tory stimulus is associated with gastrointestinal discomfort, and it causes
rejection of the food or stimulus after that point. It can be established accord-
ing to two different procedures. In the first, concurrent (short-term) TAL
(Arnedo, Gallo, Agüero, & Puerto, 1990), two gustatory stimuli are offered
simultaneously on a daily basis, and one of them is paired with an aversive
stimulus that is administered intragastrically at the time ingestion takes
place. In the second, sequential (long-term) TAL, two gustatory stimuli are
offered, one each on alternate days, and one of them is paired with an aversive
stimulus administered intragastrically after a delay.
The two behavioral procedures seem to involve different anatomical struc-
tures (Arnedo et al., 1990). Specifically, vagal lesions at the subdiaphragmatic
level and lesions in the medulla oblongata (Arnedo et al., 1990; Arnedo, Gallo,
Agüero, & Puerto, 1991; Arnedo, Gallo, Agüero, Molina, & Puerto, 1993) and
medial parabrachial nucleus (mPBN) (Agüero, Gallo, Arnedo, Molina, &
Puerto, 1996, 1997) disrupt concurrent TAL, while lesions in the area pos-

This work was submitted by the first author as a partial fulfillment of the requirements for a
Ph.D. degree in Psychology (Psychobiology), University of Granada, Granada, Spain, 1995.
Our thanks to Ms. Mary Frances Litzler for her help in the English version of this text.
Correspondence should be addressed to C. Mediavilla, Area de Psicobiologı́a, Departamento de
Psicologı́a Experimental y Fisiologı́a del Comportamiento, Universidad de Granada, Campus de
Cartuja, Granada 18071, España. Fax: (958) 246239. E-mail: cristina@platon.ugr.es.

13 1074-7427/99 $30.00
Copyright © 1999 by Academic Press
All rights of reproduction in any form reserved.
14 MEDIAVILLA, MOLINA, AND PUERTO

trema (AP) (Bernstein, Chavez, Allen, & Taylor, 1992; Coil & Norgren, 1981;
Gallo, Arnedo, Agüero, & Puerto, 1991; Ritter, McGlone, & Kelley, 1980) and
lateral parabrachial nucleus (lPBN) (Agüero, Arnedo, Gallo, & Puerto, 1993a,
b) impair sequential TAL. In this regard, a recent study conducted in our
laboratory (Mediavilla, Molina, & Puerto, in press) demonstrates the impor-
tance of the cerebellum in TAL; lesions limited to the interpositus-dentate
region block concurrent TAL, but they do not prevent development of sequen-
tial TAL.
Various authors (Eccles, 1977; Glickstein & Yeo, 1990; Ito, 1993; Marr, 1969;
McCormick & Thompson, 1984; Thompson, 1986) have proposed that the
cerebellum is the neurobiological candidate responsible for certain types of
learning and memory. Specifically, Thompson and associates have established
the anatomical pathways that unconditioned stimuli (US) and conditioned
stimuli (CS) follow during conditioning of the nictitating membrane (Kim &
Thompson, 1997; Lavond, Kim, & Thompson, 1993; Thompson, Clark,
Donegan, Lavond, Madden, Mamounas, Mauk, & McCormick, 1984; Thompson
& Krupa, 1994). The US are processed via the climbing fibers that originate in
the dorsal accessory region of the inferior olive nucleus (IO) and preferably
project to the deep nuclei of the cerebellum (Courville, Augustine, & Martel,
1977; Groenewegen & Voogd, 1977; Kitai, McCrea, Preston, & Bishop, 1977)
and HVI lobe of the cerebellar cortex (Van Ham & Yeo, 1992). Lesions in the
IO prevent acquisition of the conditioned response (CR) and facilitate extinc-
tion of previously established CRs (McCormick, Steinmetz, & Thompson, 1985;
Mintz, Lavond, Zhang, Yun, & Thompson, 1994), while electrical stimulation
of the dorsal accessory olive acts as an effective substitute for the US, which
enables learning of the CR to take place (see Thompson, 1988). Electrophysi-
ological recordings have also confirmed that IO activity is most likely related
to the acquisition process (Gruart, 1993; Sears & Steinmetz, 1991).
In terms of TAL, although little is known about the anatomical pathway
followed by gustatory information to reach the cerebellum (Hanamori, Na-
kashima, & Ishiko, 1986; Hanamori & Ishiko, 1987; Scalera & Benassi, 1989),
evidence suggests that visceral information processed by the vagus nerve may
reach it via the climbing fibers that originate in the IO (Nisimaru, Okahara, &
Nagao, 1991). In fact, the IO region may also receive information from visceral
organs by way of splanchnic and vagal afferents (Perrin & Crousillat, 1980).
Specifically, electrical stimulation of the vagus nerve induces C-fos expression
in the IO complex (Tong, Robertson, & Brons, 1991; Yousfi-Malki & Puizillout,
1994).
Because, as mentioned previously, the cerebellum seems to participate in
establishing concurrent TAL (Mediavilla et al., in press) it could be suggested
that lesions in the IO nucleus may impair concurrent TAL in a manner similar
to the way the vagal pathways are interrupted (Arnedo et al., 1990, 1991,
1993). On the other hand, IO lesions may not affect the establishment of
sequential TAL since this modality of learning uses different (nonvagal) ana-
tomical pathways (Arnedo et al., 1991; Ritter et al., 1980).
Also, in this paper we have examined the possible role of the cerebellar
cortex in concurrent TAL since a number of studies have assigned the cortex a
modulating role in autonomic functions (Squire, 1987; Supple, Leaton, &
Fanselow, 1987; Supple & Leaton, 1990; Supple & Kapp, 1993), and some
authors feel that it could be related to the establishment of motor learning
 INFERIOR OLIVE AND CONCURRENT TAL 15

(Eccles, 1977; Glickstein & Yeo, 1990; Ito, Sakurai, & Tongroach, 1982; Marr,
1969). Previous anatomical studies indicate that the vagal afferents are most
likely related to the Purkinje cells of the vermis (Tong et al., 1991), in which
case vagal-visceral information would reach regions of the posterior vermis
(lobes VI to IX) (Okahara & Nisimaru, 1991; Saigal, Karamanlidis, & Voogd,
1980), and mainly the area around the primary fissure (lobes V and VI) (Dell
& Olson, 1951; Hennemann & Rubia, 1978; Perrin & Crousillat, 1985; Tong et
al., 1991).
Despite these data, previous studies have shown that lesions in the rat
vermis do not seem to affect TAL when LiCl is used as an aversive agent and
there is a 30-min delay between ingestion of the gustatory stimulus and
administration of the aversive visceral stimulus (Supple et al., 1987). In other
words, the vermis does not appear to be essential in sequential TAL, regardless
of the possibility that cerebellar structures may be important in concurrent
tasks. This control group is especially relevant since we cannot rule out the
possibility of any motor deficits that might be overlooked or the existence of
any unspecific effects of lesions in the IO that could prevent the animals from
processing gustatory-olfactory stimuli.
In order to examine these alternatives and the negative TAL results ob-
tained after cerebellar lesioning (Supple et al., 1987), the same IO-lesioned
animals and the control group were submitted to a sequential TAL task using
new gustatory stimuli.

METHOD

Subjects
Twenty-seven male Wistar rats weighing between 260 and 350 g at the
beginning of the study were used. Eight of the animals were included in the
experimental group (IO-lesioned), another 8 made up the control group (sham-
lesioned), and the remaining 11 were lesioned in the cerebellar cortex.
All of the animals were housed individually in methacrylate cages measur-
ing 15 3 30 3 15 cm. for an adaptation period of 2–3 days during which time
food and water were available ad libitum. The room temperature was main-
tained between 21 and 24°C, and the light and dark periods lasted 12 h each.
The lights were turned on from 9:00 AM to 9.00 PM, and all experimental testing
took place during this period.

Surgery
Electrolytic lesioning of the inferior olive. Surgery was conducted under
anesthesia with sodium pentothal (sodium thiopental, Abbott Laboratories)
using a monopolar electrode approximately 200 mm in diameter. The stereo-
taxic coordinates of the IO (A-P, 23; L, 60.7; V, 20.7) were obtained from
Paxinos & Watson (1986), and 1.5 mA of cathodic current was applied bilat-
erally for 10 seconds using a DCML-5 lesion generator (Grass Instruments
Corp., Quincy, MA). All of the above steps were also followed for the sham-
lesion control group. However, the vertical coordinate of 0.7 was used and no
current was applied.
Electrocauterization of the cerebellar cortex. Once each animal had been
anesthetized and placed in a stereotaxic instrument, the point corresponding
16 MEDIAVILLA, MOLINA, AND PUERTO

to the antero-posterior coordinate 24.2 and lateral coordinate 0.0 of Paxinos &
Watson’s atlas (1986) was located in its brain. An opening was then bored to
access the surface of the cerebellar cortex with the heat source. Electrocauter-
ization lasted a total of 30 s in each case.

Intragastric Fistulae
After the brain surgery had been completed, two intragastric fistulae (Silas-
tic, Silastic-Medical Grade Tubing, Dow Corning Corp., MI) were implanted
while the animals were still under anesthesia (at times it was also necessary
to administer ethyl ether, Lab. Quimón, Barcelona). Two subcutaneous tun-
nels, one on each side of each animal, were bored through a small dorsal
opening immediately under its head; the free ends of the fistulae came out of
these tunnels. To prevent any possible infections, both the experimental and
the control animals received an im 0.1 cc dose of penicillin (Penilevel Retard,
Level Lab., S.A. Barcelona).

Concurrent TAL Behavioral Procedure

A period of 7–10 days was allowed for postoperative recovery. Afterward, the
animals were given 3 days of training during which time they were placed on
a 23 h 53 min water deprivation schedule and allowed to drink tap water from
two graduated burettes for the remaining 7 min only. The burettes were
offered simultaneously to prevent development of any positional preferences
and to train the animals to alternate between them. Thirty minutes later, the
subjects were provided 15 g of food (Panlab, S.L. Barcelona).
Experimental testing began after the 3-day adaptation period. In each trial,
the rats were given a choice of two gustatory stimuli offered at the same time
(0.5% strawberry (S) and 0.5% coconut (C), McCormick Co. Inc., San Francisco,
CA). Ingestion from one burette was paired with simultaneous intragastric
injection of an aversive stimulus, hipertonic NaCl (5%), while ingestion from
the other was paired with physiological saline (PS) administered via the other
fistula. Both stimuli were administered at a rate of 1 ml paired substance/1 ml
gustatory stimulus ingested. Upon completion of the 7 min of experimentation,
the burettes were removed and a record was made of the amounts of each
gustatory stimuli that had been consumed.
In order to compensate any natural taste preferences of the subjects, the
aversive substance was properly balanced; half of the animals received the
aversive stimulus when they drank S and saline when they drank C, while the
other half received the aversive stimulus paired with C and saline paired with
S. A graphic reproduction of this procedure has already been published
(Arnedo et al., 1991).
Each of the five experimental sessions in this concurrent TAL paradigm was
considered a discriminatory trial in itself because the animals had to deter-
mine rapidly which gustatory stimulus was associated with the aversive stim-
ulus that caused gastrointestinal stimulation.

Sequential TAL Behavioral Procedure

Once the concurrent task had been completed, the rats were allowed a period
of 48 h with food and water available ad libitum. After this period a 23 h 53 min
deprivation schedule was imposed again and a second 2-day experiment was
 INFERIOR OLIVE AND CONCURRENT TAL 17

begun. Each of the two different gustatory stimuli (0.5% vanilla (V) and 0.5%
lemon (L), McCormick Co, Inc.) was offered on alternate days for 7 min, so the
subjects had access to only one of the two stimuli per session. For half of the
animals ingestion of one flavor (the two were appropriately balanced) was
followed 15 min later by intragastric administration of 5 ml of LiCl (0.15 M,
Gruppo Montedison, Carlo Erba, Milán), and ingestion of the other stimulus
was paired with physiological saline. Thus, half of the animals received LiCl
after drinking V, while the other half received it after drinking L.
After one acquisition trial, the choice tests were offered on Day 3. Test 1
involved presentation of two burettes containing the same gustatory stimuli
that had been associated with LiCl and saline during the acquisition trials, but
this time they were offered simultaneously for the 7 min of the experiment.
Test 2 took place 6 h later; at this point the lesioned and sham-lesioned control
group again had access to the same two gustatory stimuli for 7 min, but the
positions of the two burettes were reversed, when they had been maintained
throughout the acquisition trials and Test 1.

Histology
The animals in the lesioned groups were sacrificed by an overdose of sodium
pentothal and intracardially perfused. Their brains were then extracted and
placed in formaldehyde for at least 1 week and frozen. Finally, the correspond-
ing regions were sliced (40 mm), set, stained with cresyl violet, and examined
under a microscope to determine the location and extent of the lesions.

RESULTS

Concurrent TAL
Ingestion of the stimuli by each of the groups was analyzed using an ANOVA
(days 3 drugs). The result of this analysis shows that the effect of days (F(4,28)
5 2.21, p . .05), the effect of drugs (F(1,7) 5 0.81, p . .05), and the interaction
of trials 3 drugs (F(4,28) 5 0.99, p . 0.05) were not significant for the
IO-lesioned animals (Fig. 1). By contrast, the sham-lesioned control group was
clearly able to learn it and consumed more of the gustatory stimulus paired
with PS, as seen in the statistical analysis which showed a significant differ-
ence for the main effect (F(1,7) 5 7.63, p , 0.03) (Fig. 2). The cerebellar
cortex-lesioned group also learned the task and consumed significantly more of
the PS-paired gustatory stimulus, as the interaction of trials 3 drug was
significant (F(4,40) 5 3.08, p , .03). In fact, on the fourth and fifth days, the
control animals had already ingested significantly more of the stimulus asso-
ciated with PS, ANOVA (aversive vs nonaversive) t 5 2.13, p 5 0.05; and t 5
3.82, p , 0.005 (Fig. 3).

Sequential TAL
The results of the trials were analyzed using an ANOVA (aversive vs nona-
versive condition) and indicate that both the lesioned group (x# 5 0 vs x# 5 8.1;
F(1,7) 5 72.53, p , .0002) and the sham-lesioned group (x# 5 0.6 vs x# 5 6.7;
F(1,7) 5 20.57, p , .003) were able to learn the task (Fig. 4A). The two groups
also showed a preference for the stimulus paired with PS in the reversal trial:
18 MEDIAVILLA, MOLINA, AND PUERTO

FIG. 1. Mean intake of the gustatory stimuli paired with NaCl and PS in concurrent TAL. PS,
physiological saline.

lesioned group (x# 5 0 vs x# 5 10.9; F(1,7) 5 207.86, p , .0001); control group (x#
5 1.6 vs x# 5 8; F(1,7) 5 7.52, p , .03) (Fig. 4B).

Histology
The cortical lesions were located in the region around the primary fissure
and included lobes V and VI of the vermis. The vertical and antero-posterior
extent of the lesions can be seen in the sagittal section of the cerebellum (Fig.
5), and the lateral extent can be observed in the transversal section (Fig. 6).
The wide bilateral electrolytic lesions of the IO (Fig. 7), on the other hand, do
not allow specification of the critical region but do include the medial accessory
olive (MAO), a region proposed mainly as a relay nucleus for vagal information
(Nisimaru et al., 1991; Perrin & Crousillat, 1980; Yousfi-Malki & Puizillout,
1994).

DISCUSSION

Electrolytic lesions in the inferior olive of rats impair concurrent TAL when
intake of the gustatory stimulus and administration of the visceral stimulus

FIG. 2. Mean intake of the gustatory stimuli paired with NaCl and PS in concurrent TAL. PS,
physiological saline.
 INFERIOR OLIVE AND CONCURRENT TAL 19

FIG. 3. Mean intake of the gustatory stimuli paired with NaCl and PS in Experiment 1
(concurrent TAL). PS, physiological saline.

take place simultaneously. Accordingly, in order for intake and administration

to occur at the same time, the visceral stimulus must be processed rapidly. It
appears that this requirement can be achieved by way of a neural pathway. In
fact, it has been demonstrated that the vagus nerve and related mPBN may be
critical anatomical structures involved in concurrent TAL (Arnedo et al., 1990,
1993; Agüero et al., 1997).
Because the same lesioned animals are able to learn a sequential TAL task,
it could be suggested that the IO lesions did not interfere with processing of the
gustatory information. Also, any possibility that the impairment of learning
might be attributed to the task difficulty or to the fact that the animals had
lesions could also perhaps be ruled out. Nevertheless, despite a new procedure
as well as the new taste-aversive stimuli used in this second test, we cannot
exclude the probability of a carryover effect. However this carryover effect was
not observed after lesions in the interpositus-dentate region (Mediavilla et al.,
in press).
The data for the control group, and especially for the cerebellar cortex-
lesioned group, show that the concurrent TAL task is achievable in the case of
lesioned animals. Similar findings have been reported for animals with lesions
in the area postrema (Arnedo et al., 1990) and lateral parabrachial nucleus
(Agüero et al., 1997).
At the same time, the reversal test involving sequential TAL seems to rule
out any motor alterations. In this trial, the gustatory stimuli are offered in the
exact opposite positions to those used during the learning process so the
animals must modify their previous motor programs by adjusting to the
gustatory nature of the stimuli in new positions. Both the control and the IO
lesioned animals make the adjustment.
Nevertheless, it can be argued that the aversive stimulus administered in
the sequential task (LiCl) may be stronger than the stimulus used in the
concurrent test (NaCl). In this regard, we were able to determine that, al-
though sequential learning can also be established by administering NaCl to
20 MEDIAVILLA, MOLINA, AND PUERTO

FIG. 4. Mean intake of the gustatory stimuli paired with LiCl and PS in Test 1 (A) and Test
2 (B) (reversal) of Experiment 2 (sequential TAL). PS, physiological saline.

animals lesioned in the interpositus-dentate region of the cerebellum (Media-

villa et al., in press) and vagotomized in the medulla oblongata (Arnedo et al.,
1993), this is not the case when LiCl is used (regardless of the dose) to develop
concurrent TAL (Arnedo et al., manuscript in preparation). In fact, LiCl has
consistently been found to be inadequate for the development of concurrent
TAL. In this regard, Niijima and Yamamoto (1994) have shown that LiCl
administered intraduodenally elicits afferent responses in the vagal nerve
with an onset latency of 5–10 min (see also Yamamoto, Shimura, Sako, Ya-
soshima, & Sakai, 1994). These results are in agreement with the findings by
Martin et al. (1978) and our own results that suggest that the vagus nerve is
not involved in LiCl-induced TAL. Thus, correct execution of concurrent and
sequential procedures cannot be attributed to the greater or lesser aversive
strength of the stimuli administered intragastrically. The aversive strength of
one stimulus compared to that of another is not an absolute value in TAL, but
 INFERIOR OLIVE AND CONCURRENT TAL 21

FIG. 5. Representative photomicrograph of sagittal section of the cerebellum showing antero-

posterior extension of lesion of cerebellar cortex.

rather a relative one, and it depends on the type of learning (concurrent or

sequential).
Lesioning of the IO could, therefore, have interrupted transmission of the
visceral information, which should have reached the cerebellum through the

FIG. 6. Representative photomicrograph of transverse section through the cerebellum show-

ing lateral extension of lesion of cerebellar cortex.
22 MEDIAVILLA, MOLINA, AND PUERTO

FIG. 7. Representative photomicrograph of transverse section of medulla oblongata showing

electrolytic lesion of inferior olive.

vagus nerve. This conclusion would be supported by anatomical data that

suggest that the olive region is a relay nucleus for vagal afferents. In this
regard, recent studies using electrophysiological methods (Okahara & Nisi-
maru, 1991; Perrin & Crousillat, 1985; Tong et al., 1991), peroxidase (Fitzak-
erley & Lucier, 1988; Nisimaru et al., 1991), and C-fos expression (Yousfi-
Malki & Puizillout, 1994) confirm that the inferior olive region is a relay
nucleus for vagal afferents heading toward the cerebellum. The precise con-
nections of the vagal-olivary cerebellar fibers are not known (Tong et al., 1991),
but they could include the nucleus of the solitary tract since there is a direct
projection from caudal regions of this nucleus toward ipsilateral olivary nuclei,
specifically, the dorsal accessory olive (Loewy & Burton, 1978). The functional
role of these vagal afferents has not been clarified sufficiently, but they have,
however, been related to the visceral activity of nausea and vomiting in cats
(Tong et al., 1991).
Participation of the cerebellum in autonomic functions was suggested by
Moruzzi in the 1940s and later confirmed by Dell and Olson (1951). More
recently, Hennemann and Rubia (1978) found that stimulation of the vagus
nerve actually evoked potentials in lobes V and VI of the cerebellum. This
 INFERIOR OLIVE AND CONCURRENT TAL 23

vagal information may reach the deep nuclei of the cerebellum through the IO
since numerous cells in this region IO send their fibers to the cerebellar cortex
and deep nuclei region (Qvist, 1989). In fact, electrical stimulation of accessory
olive regions causes postsynaptic excitatory potentials in the anterior inter-
positus nucleus (Kitai et al., 1977). In addition, degeneration and autoradiog-
raphy techniques have shown that the contralateral accessory olive sends
fibers to the interpositus nucleus (Groenewegen & Voogd, 1977) and, in gen-
eral, to all of the nuclear cells under the influence of the Purkinje cells that
receive climbing fibers from this specific area of the IO (Courville et al., 1977).
The data presented in this article are supported by a parallel study (Media-
villa et al., in press) that shows that the interpositus-dentate region of the
cerebellum may be a key location for the establishment of concurrent TAL
since lesions in the region interrupted this type of TAL.
The present study demonstrates for the first time that cerebellar circuits
are involved in TAL, as in other types of learning such as motor learning
(Rondi-Reig, Delhaye-Bouchaud, Mariani, & Caston, 1997), conditioning of
the patellar reflex in cats (Voneida, Christie, Bogdanski, & Chopko, 1990),
conditioning of the nictitating membrane in rabbits (McCormick et al.,
1985; Mintz et al., 1994), and others. Similarly, these studies have consis-
tently demonstrated that electrolytic and chemical lesions in the inferior
olive complex have suppressed previously established conditioned re-
sponses and prevented acquisition of new CRs (McCormick et al., 1985;
Mintz et al., 1994). The explanation offered is that destruction of olive
nuclei prevents information on the unconditioned stimulus from reaching
the cerebellum through the climbing fibers.
Finally, the results of the cortical-lesioned group deserve additional com-
ment in this context since different results have been obtained and different
interpretations have been offered for conditioning of the nictitating membrane
when the cerebellar cortex has been lesioned (Clark & Lavond, 1994; Der-
sarkissian, Logan, & Thompson, 1995; Glickstein, 1992; Hardiman & Yeo,
1992; Harvey, Welsh, Yeo, & Romano, 1993). Given all of this information, we
cannot conclude at the present time that the cerebellar cortex is not necessary
for concurrent TAL and, on the contrary, it appears to meet the essential
requirements for participating in the acquisition process, as can be deduced
from anatomical, electrophysiological, and other behavioral studies (Black,
Isaacs, Anderson, Alcantara, & Greenough, 1990; Kim & Thompson, 1997;
Schreurs, Sanchez-Andres, & Alkon, 1991). Nevertheless, the animals were
able to complete the task correctly, even though the conditions for lesioning the
(vagal) cerebellar cortex had apparently been met. In any case, our results do
not allow us to determine whether the cerebellar cortex is involved in TAL at
this point since there is always the possibility that some crucial regions of the
cortex may have remained intact.
Our data do seem to differentiate once again between the two TAL para-
digms used in our laboratory, which we consider to be separate learning
systems with different anatomical structures. This dissociation is analogous to
others found by authors who use different learning paradigms (Gabriel, Kang,
Poremba, Kubota, Allen, Miller, & Steinmetz, 1996; Packard & McGaugh,
1992; Squire, 1986; Squire, & Zola-Morgan, 1988).
24 MEDIAVILLA, MOLINA, AND PUERTO

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