Article

The expression of social dominance following neonatal lesions of the amygdala or hippocampus in rhesus monkeys (Macaca mulatta)

Université de Fribourg, Freiburg, Fribourg, Switzerland
Behavioral Neuroscience (Impact Factor: 2.73). 09/2006; 120(4):749-60. DOI: 10.1037/0735-7044.120.4.749
Source: PubMed
ABSTRACT
As part of ongoing studies on the neurobiology of socioemotional behavior in the nonhuman primate, the authors examined the social dominance hierarchy of juvenile macaque monkeys (Macaca mulatta) that received bilateral ibotenic acid lesions of the amygdala or the hippocampus or a sham surgical procedure at 2 weeks of age. The subjects were reared by their mothers with daily access to large social groups. Behavioral observations were conducted while monkeys were given access to a limited preferred food. This testing situation reliably elicited numerous species-typical dominance behaviors. All subjects were motivated to retrieve the food when tested individually. However, when a group of 6 monkeys was given access to only 1 container of the preferred food, the amygdala-lesioned monkeys had less frequent initial access to the food, had longer latencies to obtain the food, and demonstrated fewer species-typical aggressive behaviors. They were thus lower ranking on all indices of social dominance. The authors discuss these findings in relation to the role of the amygdala in the establishment of social rank and the regulation of aggression and fear.

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The Expression of Social Dominance Following Neonatal Lesions of the
Amygdala or Hippocampus in Rhesus Monkeys (Macaca mulatta)
M. D. Bauman, J. E. Toscano, and W. A. Mason
University of California, Davis
P. Lavenex
University of California, Davis, and Universite´ de Fribourg
D. G. Amaral
University of California, Davis
As part of ongoing studies on the neurobiology of socioemotional behavior in the nonhuman primate, the
authors examined the social dominance hierarchy of juvenile macaque monkeys (Macaca mulatta) that
received bilateral ibotenic acid lesions of the amygdala or the hippocampus or a sham surgical procedure
at 2 weeks of age. The subjects were reared by their mothers with daily access to large social groups.
Behavioral observations were conducted while monkeys were given access to a limited preferred food.
This testing situation reliably elicited numerous species-typical dominance behaviors. All subjects were
motivated to retrieve the food when tested individually. However, when a group of 6 monkeys was given
access to only 1 container of the preferred food, the amygdala-lesioned monkeys had less frequent initial
access to the food, had longer latencies to obtain the food, and demonstrated fewer species-typical
aggressive behaviors. They were thus lower ranking on all indices of social dominance. The authors
discuss these findings in relation to the role of the amygdala in the establishment of social rank and the
regulation of aggression and fear.
Keywords: amygdaloid complex, social behavior, fear, aggression, macaque monkey
The primate amygdala has historically been implicated in a
variety of behaviors associated with species-typical social behav-
ior (Kling, 1992). Recent evidence indicates that selective damage
to the amygdala does not disrupt fundamental components of
social behavior, such as the ability to produce and respond to
species-typical social signals and the ability to interact in a social
context. However, bilateral amygdala lesions do alter several fac-
ets of social interactions, such as affiliation, aggression, and fear
behaviors (Bauman, Lavenex, Mason, Capitanio, & Amaral,
2004a, 2004b; Emery et al., 2001; Prather et al., 2001). Thus, the
amygdala may play a role in complex social interactions that
depend on the ability to correctly regulate aggression, affiliation,
and fear responses. These behaviors are essential for the formation
and maintenance of a social dominance hierarchy (Sade, 1967).
Most species of macaques demonstrate well-defined dominance
hierarchies in both free-ranging (Drickamer, 1975) and captive
social groups (Bernstein & Mason, 1963; Janus, 1992). Dominance
relationships among primates are defined by the history of previ-
ous agonistic encounters. The pattern of previous encounters al-
lows accurate prediction of future interactions between two o
r
more individuals (Bernstein, 1981). From an ethological perspec-
tive, an animal’s ability to recognize social attributes and predic
t
the outcome of a social encounter undoubtedly serves an adaptive
function of minimizing injuries that might be sustained through
aggressive conflicts (Bernstein, 1981). Indeed, macaques have
developed a sophisticated repertoire of social signals that can be
used to define and reinforce dominance relationships (Altmann,
1967; Missakian, 1972; Sade, 1967). These signals presumably
evolved as an adaptation for successfully living within a social
group (Cheney, Seyfarth, & Smuts, 1986).
It is likely that several brain systems are involved in regulating
the production and interpretation of species-typical social signals,
including appropriate dominant and subordinate responses (Reader
& Laland, 2002). In the primate, substantial attention has been
directed to the amygdala, because its damage leads to clea
r
changes in dominance status. Rosvold, Mirsky, and Pribram
(1954) first evaluated the role of the amygdala in social rank by
lesioning the amygdalae of the 3 highest ranking male members o
f
M. D. Bauman and D. G. Amaral, Department of Psychiatry and
Behavioral Sciences, Center for Neuroscience, California National Primate
Research Center, and The M.I.N.D. Institute, University of California,
Davis; J. E. Toscano, Department of Psychiatry and Behavioral Sciences,
Center for Neuroscience, and California National Primate Research Center,
University of California, Davis; W. A. Mason, Department of Psychology
and California National Primate Research Center, University of California,
Davis; P. Lavenex, Department of Psychiatry and Behavioral Sciences,
Center for Neuroscience, California National Primate Research Center, and
The M.I.N.D. Institute, University of California, Davis, and Institut de
Physiologie, Universite´ de Fribourg, Fribourg, Switzerland.
This research was supported by National Institute of Mental Health
Grant R37MH57502 and by the base grant (RR00169) of the California
National Primate Research Center (CNPRC). This work was also supported
through the Early Experience and Brain Development Network of the
MacArthur Foundation. We thank the veterinary and husbandry staff of the
CNPRC for excellent care of the animal subjects. We also thank Jeffrey
Bennett and Pamela Tennant for assistance with surgical procedures and
Melissa Marcucci for assistance with behavioral data collection.
Corresponding concerning this article should be addressed to D. G.
Amaral, The M.I.N.D. Institute, University of California, Davis, 2825 50th
Street, Sacramento, CA 95817. E-mail: dgamaral@ucdavis.edu
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Published in "Behavioral Neuroscience 120(4): 749-760, 2006"
which should be cited to refer tothis work.
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a small social group of macaques. Following amygdalectomy, 2 of
the 3 previously high-ranking monkeys became submissive and
fell to the bottom of the dominance hierarchy, whereas the 3rd
monkey became abnormally aggressive. Similar decreases in so-
cial dominance following bilateral amygdala damage have been
reported in other primate species (Kling, 1992; Kling & Cornell,
1971; Plotnik, 1968). The underlying causes of the fall in domi-
nance remain unclear. However, several possible explanations
have been proposed, including social disinterest, rejection by other
group members, and/or an inability to correctly produce and in-
terpret social signals.
Though amygdala damage may play a role in maintaining social
dominance in adult subjects, it is not known what effect neonatal
lesions may have on the initial formation of species-typical dom-
inance hierarchies in younger subjects. Previous research on neo-
natal amygdala lesions has suggested that early damage to the
amygdala may have enduring consequences on social develop-
ment, though methodological issues, such as rearing conditions
and lesion techniques, may complicate the interpretations of be-
havioral data (Bachevalier, 1994; Prather et al., 2001; Thompson,
Schwartzbaum, & Harlow, 1969). Thompson and colleagues first
reported that individually reared female rhesus monkeys who had
sustained bilateral amygdala lesions early in life were abnormally
fearful of conspecifics during the first year of development and
abnormally subordinate to control subjects when observed at 3 and
6 years of age (Thompson, Bergland, & Towfighi, 1977; Thomp-
son et al., 1969). However, it is not known whether the abnormal
subordinate behavior associated with early amygdala damage
would be observed in a more naturalistic social-rearing environ-
ment, as differences in rearing conditions have long-lasting effects
on the acquisition of dominance rank in rhesus monkeys (Bastian,
Sponberg, Suomi, & Higley, 2003; Mason, 1961).
As part of our ongoing evaluation of the role of the amygdala in
the development of social behavior, we have examined the social
dominance hierarchy of juvenile rhesus monkeys that had received
bilateral lesions of either the amygdala or hippocampus or a sham
procedure at 2 weeks of age. Our lab has previously reported that
these neonatally amygdala-lesioned monkeys developed the fun-
damental components of social behavior (Bauman et al., 2004b). It
is unknown whether early amygdala damage may alter more
sophisticated social interactions, such as the establishment of so-
cial rank. To evaluate the role of the amygdala in dominance-
related behaviors, we provided the juvenile groups (mean age of 18
months) with a limited resource (i.e., a preferred food) that com-
monly induces agonistic behaviors among macaque monkeys
(Southwick, 1967). Preferential access to food is an indication of
social dominance, as the most dominant members of a group will
generally gain initial access to a restricted food resource (Belzung
& Anderson, 1986). We predicted that if the amygdala is involved
in the regulation of species-typical dominance behaviors, we
would observe less access to the food, indicating lower social rank
among the amygdala-lesioned subjects.
Method
All experimental procedures were developed in consultation with the
veterinary staff at the California National Primate Research Center. All
protocols were approved by the University of California, Davis, Institu-
tional Animal Care and Use Committee.
Subjects and Living Conditions
Twenty-four infant rhesus monkeys (Macaca mulatta) naturally born of
multiparous mothers were randomly assigned to one of three lesion con-
ditions: bilateral amygdala lesions (5 females, 3 males), bilateral hip-
pocampus lesions (5 females, 3 males), or sham-operated controls (4
females, 4 males). All surgeries were performed 12–16 days after birth.
The infants were returned to their mothers following surgery and provided
daily access to a socialization group consisting of 6 mother–infant pairs
and 1 adult male that interacted for a minimum of 3 hr per day, 5 days per
week. The four socialization groups were each composed of 2 amygdala-
lesioned infants and their mothers, 2 hippocampus-lesioned infants and
their mothers, and 2 sham-operated infants and their mothers. The age
range between the youngest and oldest infant within each group was
approximately 2 months. Three of the socialization groups were composed
of 1 male and 1 female per lesion condition, and the fourth cohort consisted
of 2 female amygdala-lesioned infants, 2 female hippocampus-lesioned
infants, and 1 male and 1 female sham-operated infant.
When the youngest subject within a socialization group reached 6
months of age, the infants were permanently separated from their mothers
but otherwise continued to experience the same housing and group social-
ization in the absence of their mothers. At this time, a new adult female was
added to each socialization cohort to provide ongoing exemplars of adult
female social behavior. At approximately 1 year of age, subjects became
permanently socially housed (24 hr per day) with their original socializa-
tion cohort in a chain-link enclosure (2.13-m width 3.35-m diameter
2.44-m height). The mean age of subjects at the start of dominance testing
was 1 year and 6 months, and their mean weight was 2.91 0.348 kg.
There was no significant difference in age and weight between experimen-
tal groups prior to the first and second phases of testing. Subjects had lived
in their permanent social cohorts for approximately 5 months prior to the
first phase of dominance testing.
It is important to note that one of the original male amygdala-lesioned
subjects died at approximately 1 year of age because of health reasons
unrelated to the lesion procedure and was replaced with an alternative
neonatally amygdala-lesioned male. The replacement male had been reared
alone with his mother for 10 months. Following weaning, he was housed
with an age-matched female infant until being introduced to his current
cohort at approximately 1 year and 3 months of age. The replacement
subject was accepted by the social group and had lived with the cohort for
approximately 4 months prior to testing.
Surgical Procedures
The surgical procedures are summarized below and have been described
in detail in previous publications (Bauman et al., 2004a, 2004b). On the
day of surgery, the infants were initially anesthetized with ketamine hy-
drochloride (15 mg/kg im) and medetomidine (30 g/kg) and were then
placed in an MRI-compatible stereotaxic apparatus (Crist Instruments,
Damascus, MD). The infant’s brain was imaged with a General Electric 1.5
T Gyroscan magnet; 1.0-mm-thick sections were taken with a T1-weighted
inversion recovery pulse sequence (return time [TR] 21 ms, echo time
[TE] 7.9 ms, number of excitations [NEX] 3, field of view [FOV]
8 cm, matrix 256 256). From these images, we determined the
location of the amygdala or hippocampus and calculated the coordinates
for the ibotenic acid injections. Infants were ventilated, and vital signs were
monitored throughout the surgery. A stable level of anesthesia was main-
tained by using a combination of isoflurane (1.0%, varied as needed to
maintain an adequate level of anesthesia) and intravenous infusion of
fentanyl (7–10 g/kg/hr). Following a midline incision, the skin was
laterally displaced to expose the skull; two craniotomies were made over
the amygdala or the hippocampus, depending on the predetermined lesion
condition; and the dura was reflected to expose the surface of the brain.
Ibotenic acid (Biosearch Technologies, Novato, CA; 10 mg/ml in 0.1 M
phosphate buffered saline) was injected simultaneously bilaterally into the
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amygdala or hippocampus with 10-l Hamilton syringes (26-gauge bev-
eled needles) at a rate of 0.2 l per minute. Sham-operated controls
underwent the same presurgical preparations and received a midline inci-
sion, and the skull was exposed. The control animals were maintained
under anesthesia for the average duration of the lesion surgeries, and the
fascia and skin were sutured in two separate layers. Following the surgical
procedure, all infants were monitored by a veterinarian and returned to
their mothers once they were fully alert.
Lesion Analysis
T2-weighted MRIs were obtained 10 days after surgery so that we could
examine the extent of edema associated with the lesion. We evaluated the
hyperintense T2-weighted signal for each of the 16 lesion subjects to
confirm the general target and extent of the lesions (i.e., amygdala lesion
sparing the hippocampus or hippocampus lesion sparing the amygdala).
Their brains were imaged with a General Electric 1.5 T Gyroscan magnet;
1.5-mm thick sections were taken with a T2-weighted inversion recovery
pulse sequence (TR 4,000 ms, TE 102 ms, NEX 3, FOV 8 cm,
matrix 256 256). Additional lesion confirmation was provided by
T1-weighted MRIs obtained at approximately 4 years of age. The mon-
keys’ brains were scanned with a General Electric 1.5 T Signa MRI system;
1-mm-thick sections were taken with a T1-weighted three-dimensional
axial-spoiled gradient sequence (TR 22.0 ms, TE 7.9 ms, NEX 3,
FOV 16 cm, matrix 256 256).
Behavioral Observations and Statistical Analysis
Behavioral data were collected with The Observer software (Noldus,
Sterling, VA; Noldus, 1991) by trained observers demonstrating an inter-
observer reliability greater than 90% (agreements/[agreements disagree-
ments] 100). Analyses of variance followed by Fisher’s protected least
significant difference post hoc tests (with a significance level of p .05)
were used for data analyses. Because of heterogeneous variation, all
latency data were transformed with the ln(x 1) transformation to con-
form to normal distribution requirements.
Evaluation of Pretest Food Motivation
Although each subject had been given marshmallows as enrichment
throughout its life, a formal test of the willingness and motivation to
retrieve miniature marshmallows from an affixed novel container was
essential in confirming that marshmallows were indeed a preferred food
item. Therefore, 1 week prior to the dominance test, each subject’s will-
ingness to retrieve marshmallows from the food container was evaluated.
The marshmallows were placed in a plastic food container (15 cm long
13 cm wide 8 cm high) with a 4-cm circular opening located at the top.
Willingness to retrieve the marshmallows (as indicated by the frequency of
reaches into the container) was assessed in two different contexts. The first
assessed the ability of each subject to retrieve marshmallows from the food
container when removed from its social group. Subjects were temporarily
relocated to individual holding cages (61 cm long 66 cm wide 81 cm
high) within the same room and given free access to the container filled
with marshmallows during a single 15-min session. The second context
evaluated each subject’s ability to retrieve marshmallows with all members
of the cohort present (social context). To minimize competition between
subjects prior to the formal test of dominance, we attached six identical
containers filled with marshmallows to the inside of each cohort’s large
home enclosure (8 cm apart, with the bottom approximately 25 cm above
the floor). The adult male and female were first removed from the home
enclosure, and the 6 juvenile subjects were relocated to wire-mesh holding
chutes attached to the back of their home enclosure. A technician then
entered the cage and strapped the six baited containers to the front of the
cage. Once the containers were securely fastened, the first technician exited
the cage, and a second technician released all 6 subjects simultaneously
into the cage. Once released, the subjects were allowed access to the six
containers for 15 min. There were no changes in normal diet or feeding
schedules associated with these tests.
Dominance Test Procedure
Each cohort consisting of 2 amygdala-lesioned, 2 hippocampus-
lesioned, and 2 sham-operated juvenile subjects was tested in their home
enclosure (2.13-m width 3.35-m diameter 2.44-m height). Dominance
testing comprised two distinct phases, with a 5-month interval separating
Phase 1 from Phase 2. During each phase, we assessed dominance by
allowing each cohort free access to a single container filled with marsh-
mallows for a 15-min session between 1 p.m. and 2 p.m. This procedure
was repeated five additional times over a 2-week period, resulting in six
15-min sessions per cohort per testing phase.
On the day of the dominance test, the adult male and female were first
removed from the testing area, and the 6 juvenile subjects of a given cohort
were relocated to wire-mesh holding chutes attached to the back of their
home enclosure. A technician then entered the cage and strapped the baited
container to the front of the cage (25 cm above the floor). Once the
container was securely fastened in the cage and the technician exited, a
second technician released all 6 subjects simultaneously into the cage.
Subjects were allowed free access to the container for 15 min (see Figure
1). At the conclusion of the test, the container was removed and the adults
were returned to the social group.
Dominance Test Data Collection
Access to food measures. We quantified access to the preferred food
(marshmallows) by recording each subject’s latency to first approach
within arm’s reach of the container and each subject’s latency to reach its
hand into the container, as well as the order (ranging from 1 reached first
to 6 reached last) in which each of the 6 subjects of a given cohort first
reached into the container. For those instances in which a subject never
reached during a single test session, the maximum value of 6 was assigned.
Reach orders were then summed for each subject across each test session
(6 sessions per phase, 12 sessions total). As was done with reach order, if
a subject never approached or reached during the 15-min test session, the
maximum value of 900 s was assigned. An overall frequency of reaching
was also obtained by recording the number of times each subject was
observed inserting its hand into the container throughout the 15-min
session. In addition, the frequency and duration of time spent in proximity
to the container (within arm’s reach) was also recorded (see Table 1).
Access to food in the first minute of testing. Preferential access to food
is an indication of social dominance (Belzung & Anderson, 1986). Given
that the most dominant members of a group will generally gain initial
access to a restricted food resource, we conducted a separate analysis of the
food access measures described above limited to the first minute of
dominance testing.
Behavioral measures. All frequencies of species-typical agonistic be-
haviors, such as aggression, displacements, fear grimaces, and screams,
were recorded with the identity of the initiator and recipient of each
agonistic interaction noted (Table 1). A linear dominance hierarchy was
constructed for each cohort on the basis of the directionality of recorded
dyadic aggressive interactions between subjects (Bastian et al., 2003;
Higley, Mehlman, et al., 1996). Linear rank indices (1– 6) were derived by
using the formula x/(n 1), with x signifying the total number of monkeys
each subject defeated and n 1 representing the number of monkeys each
subject could possibly defeat (maximum of 5 within their respective
cohorts). A subject was considered more dominant than another subject
when it initiated more aggressive behaviors than it received during inter-
actions with that subject.
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Social Group Observations
In addition to the formal assessment of dominance, we conducted
weekly social group observations within each cohort’s home enclosure to
provide information on dominance-related behaviors under normative con-
ditions (i.e., in the absence of a preferred resource). Each subject was
observed on 40 separate occasions during 5-min focal samples. We ob-
served subjects in a predetermined pseudorandom order by using a previ-
ously described catalog of age-appropriate, species-typical behaviors (Bau-
man et al., 2004b).
Results
MRI and Histological Evaluation of Lesions
Analysis of T2-weighted coronal images obtained 10 days fol-
lowing the surgery indicated that the ibotenic acid injections were
focused in the amygdala or hippocampus as planned. This is based
on observations of the location of hyperintense signals attributed to
transient brain edema at the sight of the injection. Coronal images
through the midportion of the amygdala for all cases were illus-
trated in previous publications (Bauman et al., 2004a, 2004b). The
extent of the targeted lesion was confirmed in 1 amygdala-lesioned
subject that died because of an unrelated illness. Histological
evaluation of the brain in this case confirmed that neurons through-
out much of the amygdala were damaged bilaterally and that
extraneous damage to surrounding structures was minimal and
generally not bilaterally symmetrical (see Figure 2 in Bauman et
al., 2004b).
Analysis of a second series of structural MRIs performed when
the subjects were approximately 4 years of age provided additional
confirmation of the lesions. All 8 amygdala-lesioned subjects
demonstrated substantial bilateral damage to the amygdaloid com-
plex, as indicated by clear shrinkage of the amygdala and/or
expansion of the ventricles into space formerly occupied by the
amygdala (see Figure 2). If there was any sparing of amygdala
Figure 1. Photograph illustrating the testing enclosure in which a container was placed that allowed limited
access to a preferred food (marshmallows).
Table 1
Dominance Test Ethogram
Behavior Description
Duration behavior
Proximity to food container Within arm’s reach of the food container for more than 3 s
Frequency behavior
Contact aggression Grab, hit, bite, or slap
Approach (to food container) Directed movement within arm’s reach of container
Avoid Withdraw from the container due to the arrival of another subject
Displacement When another subject approaches and “takes the place” of the other subject
Fear grimace Upper and lower lips retracted, exposing teeth
Flee Rapid movement away from another subject
Reach Hand or arm inserted into food container
Scream High-pitched, high-intensity vocalization
Threat One or more of the following: open-mouth stare, head bob, lunge
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tissue, it was limited to the most caudal aspects of the amygdala,
perhaps including the central nucleus. Unintended damage to cor-
tex lying adjacent to the amygdala appeared to be minimal. Dam-
age to the hippocampus in the amygdala-lesioned subjects was
limited to its rostral portion. Analysis of the hippocampus lesions
revealed nearly complete bilateral damage for all cases, with
minimal sparing of the extreme rostral and caudal portions (Figure
2). Unintended damage to the amygdala was not observed in any
of the 8 hippocampus-lesion cases, and only slight damage was
found in the surrounding parahippocampal cortex in one of the
cases. Lesion parameters were designed to minimize inadvertent
damage to the amygdala or surrounding cortices.
Pretest Food Motivation
Subjects did not differ in the frequency of reaches into the
container when tested alone, F(2, 21) 0.173, p .8425, and
when tested in a group with access to multiple containers, F(2,
21) 0.846, p .4431. Thus, lesion condition did not affect the
subject’s motivation to obtain the limited preferred resource
(marshmallows).
Dominance Test Results
Overview
Although dominance testing consisted of two distinct phases of
data collection so that we could evaluate the stability of the
hierarchies over a 6-month period, there were not many significant
differences found between Phase 1 and Phase 2; thus, data were
summed across the two phases. Several indices of social domi-
nance were measured, including food access, frequency of agonis-
tic behaviors (Table 1), and the calculation of a linear dominance
hierarchy.
Access to Food
Order of food access. Experimental groups demonstrated sig-
nificant differences on the measures of initial access to food, with
the exception of approaches to the container. Lesion effects were
found for the order of reaching, F(2, 21) 19.877, p .0001;
control subjects reached before amygdala- and hippocampus-
lesioned subjects ( p .0001 and p .0023, respectively), and
hippocampus-lesioned subjects reached before amygdala-lesioned
subjects ( p .0103; see Figure 3). Lesion effects were also found
for the latency to first approach the container, F(2, 21) 9.254,
p .0013, and to first reach into the container, F(2, 21) 6.450,
p .0066. Amygdala-lesioned subjects took longer to approach
the container than did control and hippocampus-lesioned subjects
( p .0004 and p .0094, respectively), and they also took longer
to reach into the container than did control and hippocampus-
lesioned subjects ( p .0004 and p .0094, respectively).
Access to food in the first minute of testing. Experimental
groups differed markedly in their access to the food container
during the first minute of testing when competition was presum-
ably greatest (see Table 2). The total number of reaches into the
food container, for example, during the first minute of testing was
significantly different across experimental groups, with control
subjects reaching more frequently into the container than both
amygdala- and hippocampus-lesioned subjects, F(2, 21) 12.085,
p .0003; p .0001 and p .0100, respectively. Lesion effects
were also found for the number of times subjects were observed in
proximity to the container during the first minute of testing.
Control and hippocampus-lesioned subjects were more frequently
in proximity to the container than the amygdala-lesioned subjects,
F(2, 21) 5.343, p .0133; p .0044 and p .0377, respec-
tively. Lesion effects were also found for duration of proximity,
with control subjects spending more time near the food container
than both amygdala- and hippocampus-lesioned subjects, F(2,
21) 6.039, p .0085; p .0025 and p
.0419, respectively.
It is interesting to note that