Physiology & Behavior, Vol. 27, pp. 397-400. PergamonPress and BrainResearch Publ., 1981. Printedin the U.S.A.
Differential Effects of Amygdaloid
Lesions on Conditioned Taste
Aversion Learning by Rats
J O H N P. A G G L E T O N 1, M I C H A E L P E T R I D E S 2 A N D S U S A N D. I V E R S E N
Department o f Psychology, University o f Cambridge
Cambridge, CB2 3EB Great Britain
R e c e i v e d 21 A p r i l 1981
AGGLETON, J. P., M. PETRIDES AND S. D. IVERSEN. Differential effects ofamygdaloid lesions on conditioned taste
aversion learning by rats. PHYSIOL. BEHAV. 27(3) 397-400, 1981.--Rats with electrolytic lesions placed in either the
basolateral or corticomedial divisions of the amygdala acquired a conditioned taste aversion to sucrose. Comparisons with
a surgical control group indicated that damage to the corticomedial amygdala did not alter the animals' performance, while
damage in the basolateral nuclei resulted in a small but significant attenuation of the aversion. Furthermore, these amygdaloid lesions did not alter the acceptability of two quinine hydrochloride solutions (0.01% and 0.001%). The daily drinking
behavior of the rats with basolateral amygdaloid lesions appeared consistent with the hypothesis that this lesion affected
the animals' appreciation of the novelty of the sucrose solution, and hence attenuated the subsequent aversion.
Corticomedial amygdala
Basolateral amygdala
Brain lesion
Conditioned taste aversion
Quinine
METHOD
T H E mammalian amygdala is a heterogeneous structure
composed of several cytoarchitectonically distinct nuclei,
each of which possess a unique array of anatomical connections [7]. This anatomical heterogeneity may underlie a
variety of functional specializations and studies on the effects of damage to specific nuclei or groups of nuclei within
the amygdala have provided a source of such evidence. Furthermore, ontogenic and phylogenic evidence has suggested
that these nuclei may be grouped into a basolateral and a
corticomedial division [2,3].
There is consistent evidence that removal of the amygdala
in the rat will disrupt the acquisition of a conditioned taste
aversion [6], and that damage to the basolateral nuclei is
sufficient to produce this deficit [9,11]. In order to refine our
knowledge of possible functional divisions within the amygdala, the effects of lesions centered respectively in the
basolateral (BLA) and corticomedial (CMA) groups of nuclei
were compared on a conditioned taste aversion paradigm.
It has been proposed that the attenuated taste aversion
seen after amygdalectomy reflects an inability to suppress
drinking rather than a failure to learn the aversion [8]. The
tolerances of the experimental rats to a bitter tasting solution
(quinine hydrochloride) were investigated in order to differentiate these hypotheses.
Subjects
The subjects were 32 naive, male, Lister hooded rats
whose weights ranged from 240--350 g. They were housed in
similar, individual cages with ad lib laboratory chow (Dixons
Diet 41B).
Surgery
Surgery was performed under Equithesin anesthesia (3.75
mg/kg). All lesions were made by passing a 1.8 mA DC current for 10 seconds through the uninsulated tip (1.0 mm) of a
stainless steel electrode (00-gauge). The stereotaxic coordinates, taken from Bregma, were as follows: BLA group,
anterior - 0 . 8 mm, lateral 5.2 mm and horizontal - 3 . 0 mm;
CMA group, anterior - 0 . 8 ram, lateral 3.6 mm and horizontal - 3 . 8 mm. In the control rats the electrode was lowered
only as far as the amygdala, but without entering it and without passing any current. Six rats served as controls while
basolateral and corticomedial amygdaloid lesions were
produced in 13 rats respectively.
Procedure
For the duration of the experiment each rat was allowed
1Send reprint requests to current address: National Institute of Mental Health, Building 9, Room 1N 107, 9000 Rockville Pike, Bethesda, MD
20205.
2Currently at Department of Psychology, McGill University, 1205 Dr. Penfield Avenue, Montreal, Quebec, H3A lB1 and Montreal
Neurological Institute, 3801 University Street, Montreal, Quebec, H3A 2B4, Canada.
C o p y r i g h t © 1981 B r a i n R e s e a r c h P u b l i c a t i o n s Inc.--0031-9384/81/090397-04502.00/0
398
A G G L E T O N , PETRIDES A N D I V E R S E N
10 minutes drinking time, while in a test box, and deprived of
water for the remainder of the day. The test boxes had three
metal walls, painted black, a glass front and a wire grid floor.
The floor measured 30×30 cm and the box was 38 cm high.
Each box was equipped with one burette.
For the first five days the rats were offered water. This
water was replaced with a 15% sucrose solution on day 6 and
immediately after this session the rats received an intraperitoneal injection of 0.15 M lithium chloride (20 ml/kg) to induce sickness. On days 7-10 the animals received water in
the test box and by day 10 they had returned to the level of
water consumption seen prior to the lithium sickness (day 5).
On day 11 the rats were retested with the 15% sucrose solution.
Two hours after this sucrose retest the rats were returned
to the test boxes and given water for 10 minutes. On the
following day (day 12) the animals were offered a single
bottle containing a 0.01% solution of quinine hydrochloride.
This was followed two hours later by 10 minutes access to
water. On the final test day (day 13) the rats were offered a
0.001% solution of quinine hydrochloride.
-0.6
-1.2 l
RESULTS
Histological Findings
At the completion of the experiment the animals were
sacrificed and the brains fixed in 10% sucrose-Formalin,
sectioned and mounted on slides. The lesions were reconstructed from enlarged projected images of the sections. The
amygdaloid lesions of both groups were comparable in size,
the corticomedial lesions largely filling the region depicted in
Fig. I. There was, however, greater variability in the placement of the basolateral lesions, hence the zone in which
these lesions fell is larger than that of the CMA group (Fig.
1). There was variable damage to the piriform cortex in the
BLA group, and in two rats there was slight damage to the
ventral most part of the caudate-putamen. Two rats in the
CMA group sustained some damage to the hippocampus at
the posterior extremity of the amygdala.
Behavioral Findings
Table 1 presents the mean intake of each group for days
5-I1. To evaluate the acquired aversion to sucrose a suppression ratio was calculated:
sucrose intake first exposure (day 6) - sucrose intake retest (day 11)
sucrose intake first exposure (day 6)
A complete suppression of sucrose would produce a ratio of
1.0. The suppression ratios of the three groups were found to
differ (Kruskal-Wallis, H = 16.30, p<0.001 ; Fig. 2), and the
BLA rats did not suppress their intake as strongly as either
the controls (Mann-Whitney, U = 1.5, p<0.001) or the CMA
rats ( U = 19.5, p<0.001). The CMA group did not differ from
the controls (U=30.0, p>0.05).
All animals reduced their water intake on day 7, the day
following the lithium chloride injection. The ratios of the
water intakes on day 7 to those of the previous day that
water was offered (day 5) were calculated and compared.
This analysis showed that the groups differed significantly
(H =8.11, p <0.02) and that the B L A group reduced its water
intake to a greater extent than both the controls ( U = 11.5,
p<0.01) and the CMA group (U=38.5, p<0.05).
The ratios of sucrose consumption on day 6 to water intake on day 5 were also calculated and compared. This
FIG. 1. Illustration of coronal sections depicting the zones within
which all of the basolateral 0~\~)and corticomedial (/[]) amygdaloid
lesions fell. Abbreviations: ABL, lateral basal nucleus; ABM, basomedial nucleus; ACE, central nucleus; AL, lateral nucleus; AME,
medial nucleus; CLA, claustrum; CO, cortical nucleus; PIR,
piriform cortex; ST, stria terminalis; ZT, amygdalo-hippocampal
transition area.
analysis indicated that the groups differed (H=6.09, p<0.05)
and that the B L A rats drank relatively more sucrose than the
controls ( U = 15, p<0.025).
The experimental groups did not differ in the consumption of either 0.01% quinine solution (H=0.44) or 0.001%
quinine solution ( H = 1.99, Fig. 3). There was however evidence that the groups drank differing amounts of water in the
intervening session (H=15.05, p<0.002). The BLA group
drank significantly less water on day 12 than either the controls (U=4.5, p<0.002) or the CMA group (U=19.5,
p <0.002).
DISCUSSION
The results of this study provide a dissociation between
the effects of damage to the basolateral and corticomedial
amygdaloid nuclei. Lesions of the basolateral nuclei
produced a mild, but significant, attenuation of a learnt taste
aversion, while damage to the corticomedial region had no
discernible effect. The effects of basolateral amygdaloid
damage were qualitatively consistent with previous reports
[9,11], while corticomedial amygdaloid lesions had not previously been tested formally on this paradigm. The normal
reactivity of the rats with amygdaloid lesions to unpleasant
tastes, such as quinine, in this and other experiments [5, 6,
9], shows that this interference is not due to a failure to
suppress the drinking response.
Although rats with lesions in the basolateral amygdala
were impaired on the conditioned taste aversion task the
degree of this impairment appeared slight when compared to
previous studies [6, 9, 11]. A possible explanation of this
AMYGDALOID LESIONS AND TASTE AVERSIONS
399
TABLE 1
M E A N S A N D S T A N D A R D E R R O R S (S.E.) O F T H E D A I L Y F L U I D I N T A K E S (ml) O F T H E T H R E E
EXPERIMENTALGROUPS
Day 5
Day 6
Day 7
Day 8
Day 9
Day 10
sucrose
Group
water
LiC1
water
water
water
water
retest
Control
(N=6)
Mean
S.E.
12.0
0.4
11.6
0.8
9.0
0.3
12.8
0.4
12.6
0.7
13.1
0.9
0.03
0.03
Corticomedial
Amygdala
(N---13)
Basolateral
Amygdala
(N = 13)
Mean
S.E.
11.9
0.5
12.4
0.5
8.1
0.4
11.7
0.4
12.4
0.5
13.3
0.6
0.14
0.08
Mean
S.E.
10.9
0.4
13.3
0.8
5.5
0.5
9.5
0.6
10.0
0.5
10.7
0.4
1.80
0.48
I
1.00
Day 11
sucrose
C
16-
CMA
s 14v
O
"= 0.90
BLA
12-
t~
E:
¢-
10-
.o_
8-
CMA
0~
15 6 -
~ 0.80-
4-
ffl
>O
/i////
~4
0.70 -
2-
C CMA BLA
0
0.01% Quinine
Day 12
N
Controls
CMA
BLA
FIG. 2. Mean suppression ratios to the sucrose solution. Vertical
bars mark the standard error around the mean. Suppressions ratio=
Wster
Day 12
0.001% Quinine
Day 13
FIG. 3. Mean intakes of quinine hydrochloride (0.01% and 0.001%)
and water on days 12 and 13. Vertical bars mark standard error
around the mean.
sucrose intake first exposure - sucrose intake retest
sucrose intake first exposure
discrepancy lies in the extent of the amygdaloid damage. The
basolateral lesions of previous studies appear to have typically encroached upon the central nucleus, which is the primary amygdaloid recipient of gustatory inputs [10]. It is
therefore possible that additional damage to the central nucleus, or its afferent fibers, might potentiate the disruptive
effect of basolateral amygdaloid lesions.
The abnormal drinking patterns of the BLA animals, in
this and a previous experiment [9], support the hypothesis
that the conditioned taste aversion impairment reflects a
failure to respond appropriately to the novelty of the sucrose
solution, hence attenuating the subsequent aversion. Thus
the rats with basolateral amygdaloid damage showed an excessive intake of sucrose on the first day it was offered,
which contrasted with an abnormal decrease in water con-
sumption the day after lithium poisoning. A similar lack of
neophobia for novel fluids has been seen after amygdalectomy in other experiments [5,6] while the excessive decrease
in water consumption the day after lithium poisoning has
been interpreted as an overgeneralized aversion [9]. It is
possible that the low level of water intake shown by the BLA
rats on day 12, between the two quinine hydrochloride tests,
reflects a similar overgeneralized aversion.
There is additional evidence that basolateral amygdaloid
lesions will reduce neophobia in rats. Such animals will eat
novel foods in a novel environment more readily than controis [1, 12, 14]. Furthermore, just as medial amygdaloid
lesions do not interfere with a learnt taste aversion, similar
medial lesions leave other neophobic responses intact [ 1,13].
Thus there is some consistent evidence that lesions of the
basolateral amygdala are selectively disruptive in situations
where the animal is confronted by novelty, while corticomedial lesions have little or no effect.
400
AGGLETON,
PETRIDES AND IVERSEN
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