Journal of Comparative and Physiological Psychology1973, Vol. 83, No. 2, 248-269

ALTERED FOOD PREFERENCES AFTER LESIONS INTHE BASOLATERAL REGION OF THE AMYGDALA

IN THE RAT1

EDMUND T. ROLLS2 AND BARBARA J. ROLLS3

Department oj Experimental Psychology, University oj Oxford

Rats with lesions in the basolateral amygdala chose different foods fromcontrol rats in 10-min. food-preference tests. The normal rats ate primarilyfamiliar chow, while the amygdala-lesioned rats ate primarily novel foods.The lesioned rats did not select indiscriminately but showed definite prefer-ences. With repeated testing, the normal rats' preferences became similar tothose of the amygdala-lesioned rats. Food-preference tests in a disturbingenvironment suggested that the difference between the lesioned and controlgroups was not due to a general alteration in behavior such as fear. Otheraspects of ingestive behavior, such as body weight regulation, were not pri-marily altered by the lesions. The basolateral amygdala may therefore beconcerned with the selection of foods on the basis of previous experience.

Amygdaloid neurons are activated in eat-ing and drinking elicited by electrical stim-ulation of the lateral hypothalamus in rats(E. T. Rolls, 1972). This indication thatamygdaloid neurons are involved in eatingand drinking is strengthened by the findingthat the amygdaloid neurons directly excitedby the stimulation have the same absoluterefractory period as the neurons throughwhich the eating and drinking are elicited(E. T. Rolls, 1973). To investigate furtherthe role of the amygdala in eating, ingestivebehavior following amygdaloid lesions wasanalyzed, as described here. The lesion elec-trodes were aimed at the basolateral regionof the amygdala, which is the area in whichneurons were activated in the electricallyelicited eating and drinking (E. T. Rolls,1972).

Electrophysiological and behavioral stud-ies (see E. T. Rolls, 1972) support the hy-pothesis that the amygdala is involved inreinforcement. This hypothesis was utilizedin the experiments described here. A choiceof foods was given to the lesioned animals todetermine whether the reward value of dif-ferent foods measured by food preferenceis altered by the lesions.

1 This research was supported in part by theMedical Research Council. The helpful commentsof S. J. Cooper and L. Weiskrantz are gratefullyacknowledged.

2 Requests for reprints should be sent to Ed-mund T. Rolls, Department of ExperimentalPsychology, University of Oxford, Oxford, Eng-land.

3 Nee Simons.

GENERAL METHOD

Subjects

Sixty-six male hooded Lister rats and 13 malealbino Wistar rats weighing 250-300 gm. at thestart of the experiments were divided randomlyinto an experimental group of 60 animals and acontrol group of 19 animals.

Apparatus

Food-preference tests were conducted in awire-mesh rat cage with the dimensions indicatedin Figure 1. Six different foods, arranged for Ex-periment 1 as in Figure 1, were placed in blackplastic bottle tops 6 cm. in diameter. Each foodcup contained about 5 gm. of chopped food. Therat cage was placed on a table in a small room.

Procedure

The rats were maintained in individual cageswith ad-lib water. Standard laboratory chow inpellet form—Dixon's FFG(M)—was available inhoppers or on the floor of the cage. On the daybefore a food-preference test the food was removedat 1530, 2Vii hr. before the lights were extinguished(illumination was off between 1800 and 0800).

For a food-preference test, a rat was deprivedof food overnight and tested in the morning.Often the experimenter did not know whetherthe subjects were control or experimental ani-mals. A stopwatch was started when the rat wasplaced in the cage, and the time when a ratstarted and stopped eating each type of food wasnoted. Eating was denned as picking up food, bit-ing and chewing it, and ingesting it. After 10 min.the rat was removed from the cage, and the timesspent eating each type of food were determined.Laboratory chow was given to the animal muchlater, in the afternoon. A rat was tested only oncea day with a minimum of 2 days between tests.

248

FOOD PREFERENCE AFTER AMYGDALA LESIONS 249

Greens

Chow

Sultanas

Potato

Cauliflower

Eu8

50cmFIG. 1. Plan of arrangement of foods in the wire-mesh test cage. (Each food was in a container 1.0

cm. high.)

Surgery

Bilateral lesions were made in the region of thebasolateral amygdala of the experimental groupof rats.

The rats were anesthetized with an intra-peritoneal injection of 3 ml/kg of Equi-Thesin(Jensen-Salsbury Labs., Inc.). Using level-head co-ordinates, the platinum-indium lesion electrode(10% iridium, 90% platinum wire, 28 ga.) waslowered vertically to the basolateral amygdaloidregion. Coordinates ranged from 2-3.0 mm. behindthe bregma, 4.25-5.0 mm. lateral to the midline,and 7.8-8.5 mm. below the dura. Anodal currentspassed through the exposed V^-mm. electrode tipwith a foot or an ear bar as the indifferent andranged from 3 ma. for 30 sec. to 5 ma. for 60 sec.The resulting lesions are nonirritative (B. J.Rolls, 1970). At least 1 wk. (usually 2-3 wk.) wasallowed for recovery before the first food-prefer-ence test was made. Body weight and water in-take were measured daily.

Histology and Division of Animals intoGroups

At the completion of experimentation, whichincluded the tests described in B. J. Rolls andE. T. Rolls (1973), the animals were deeplyanesthetized with ether and perfused intra-cardially with .9% saline followed by 10% For-malin. In some cases 6 mo. elapsed after thelesions before the perfusion was made. The brainswere removed after at least 3 days in Formalin. Anumber of the brains were embedded in paraffinwax and 15-/u sections were stained with thionin.An alternative method, which proved successful,was to section the fixed brain manually. In eithercase, an outline of the extent of the lesion wasmade on drawings of the rat brain seen in thp

coronal plane, taken every 1 mm. from KSnig andKlippel's (1963) atlas.

On the basis of the histology the lesioned ratswere divided into two groups for the analysis ofthe data. Thirty-three rats with bilateral lesionsin the region of the lateral amygdala and pyri-form cortex formed the Am group. Thirteen ofthese 33 rats with lesions which bilaterally de-stroyed the basolateral region of the amygdalaformed the BL group. Examples of lesions in theBL group of animals are shown in Figure 2. Thelesions were in the area in which neurons activa-ted in stimulus-bound eating and drinking arefound (E. T. Rolls, 1973). The body weights andgrowth rates of the lesioned animals in the BLand Am groups were very similar to the controls(for example, in 14 days, immediately post-operatively for the lesioned groups, the Am groupgained 37 gm., the BL group 29 gm., and thecontrols gained 34 gm.). The water intakes of therats are described in B. J. Rolls and E. T. Rolls(1973). Twenty-seven lesioned rats were not in-cluded in these groups. Of these rats, 4 wereused in initial experiments; 2 grew abnormallylarge incisor teeth; 11 had either asymmetrical, orvery small, or badly positioned lesions; and 10lost weight rapidly and died or were killed within1 wk. of the lesions. These last 10 rats typicallyshowed aphagia and adipsia, and on autopsymany had a sequestration of yellow or blackfluid in the gastrointestinal tract. Their lesionswere typically large and were centered on themedial amygdaloid region but often includedparts of the internal capsule and the lateral hypo-thalamus (see Figure 2).

EXPERIMENT 1The purpose of the experiment was to de-

termine the food preferences of the amyg-dala-lesioned and control rats.

250 EDMUND T. ROLLS AND BARBARA J. ROLLS

b a

FIG. 2. (a) Examples of lesions typical of the animals with lesions in the basolateral region of theamygdala (BL group). (6) Reconstruction of lesions of the 11 rats in the BL group. (The common regiondamaged bilaterally in 8,5, and 3 of the 11 rats is shown by the contours. For example, the overlap regionof the lesions in 8 of the rats is shown by the innermost, most densely shaded area. The lesions destroyeda basolateral region of the amygdala. [Outline drawing from Konig & Klippel, 1963, Plate 37b].) (c)Reconstruction of lesions of 4 of the 10 rats which died after amygdala lesions. (The common regiondestroyed bilaterally in 3 and 2 of the 4 rats is shown by the contours. The lesions destroyed parts of thecentral and medial nuclei of the amygdala. [Outline drawing from Konig & Klippel, 1963, Figure 37b].In a further three rats the common region was 1.0 mm. further rostral at the same distance from themidline.)

ProcedureIn this first food-selection test administered

to the rats, the foods were standard chow, cauli-flower, orange peel, potatoes, sultanas, and greens(see Figure 1). The chow was identical to thatavailable in the home cages. The other foods werefresh, washed, and uncooked. They were choppedinto small portions with the maximum dimensionbeing about .5 cm. The white of the cauliflowerwas used. The potatoes were peeled. Sultanas area form of seedless white raisin. The greens were"spring greens," which are green leafy vegetables.Fresh cauliflower leaves and fresh spinach aresimilar.

Results

In all the food tests, the general behaviorof the three groups of animals was similar.

On being placed in the test cage, a rat typi-cally explored the cage for the first 30-90sec., sniffing and sometimes tasting the foodsduring this period. Then the rats started toeat the foods, typically eating a particularfood for 15 sec.-l min., then moving on toeat another food. Thus in almost all the testsevery food was sampled by the rats. Differ-ences between groups of rats arose becausesome rats repeatedly returned to a particu-lar food to eat it in preference to the otherfoods.

The three groups of animals ate for verysimilar lengths of time (controls for 196 ±21 sec., Am for 231 ± 16 sec., BL for 245 ±27 sec.). (The variance figure given through-

FOOD PREFERENCE AFTER AMYGDALA LESIONS 251

out is the SEU.) These times are not signifi-cantly different from each other (i.e., p >.05; two-tailed t tests are used throughoutthis paper).

The Am and BL groups showed very dif-ferent preferences from the controls. Thefood preferences of a rat were expressed byconverting the time spent on each food to apercentage of the rat's total eating time. InFigure 3 the percentages for each food havebeen averaged over the different animals ineach group. As well as the mean, the stand-ard deviation of the mean percentage of thetime a group of rats ate each food was alsocalculated. A two-tailed t test was used todetermine whether a group of rats ate aparticular food for a different time to an-other group of rats. The Am group ate lesschow than the controls (p < .001), moresultanas (p < .02), and more cauliflower

Test 1

(p < .05). The BL group ate less chow thanthe controls (p < .001), more sultanas (p <.01), and more cauliflower (p < .01). Otherdifferences were not significant. The alteredfood preferences were more extreme in theBL than the Am group (see Figure 3), al-though a direct comparison of the BL andthe Am groups on each of these foods justfailed to reach significance (p > .05).

Discussion

It can be concluded that the rats withamygdala lesions, particularly in the baso-lateral region of the amygdala, spent muchless time eating standard chow and moretime eating sultanas and cauliflower thanthe controls when placed in the test situa-tion for the first time.

The control group of rats ate little of theunfamiliar foods, consuming chow for 64%

Cont (19)Am (33)BL (13)

chow cauliflower sultanas potato greens orange peel

FIG. 3. Food preferences of amygdala-lesioned rats (Am and BL) and control rats. (The BL grouphad symmetrical lesions in the basolateral region of the amygdala. The number of rats in each group isindicated in parentheses. In this and subsequent figures preferences are indicated by the mean percen-tage of the total times [histograms ± SE] that the rats ate each food.)

252 EDMUND T. ROLLS AND BARBARA J. ROLLS

of the eating time. They just sampled theunfamiliar foods. It may be stressed thatthe chow was familiar because it was nor-mally available in the home cages. The ratswith amygdala lesions sampled and ate thenew foods, eating chow for only 34% (Am)or 20% (BL) of their eating time.

The control rats may have sampled theunfamiliar foods and found them unpalata-ble. Therefore, in the rats' second test (Ex-periment 2) chocolate chip cookies, whichare reputed to be highly palatable to rats(Teitelbaum & Epstein, 1962), were in-cluded in the foods to determine whethertheir palatability could coax the controlsaway from the chow. If this happened, itwould be evidence that the altered prefer-ences seen in Experiment 1 after amygdalalesions were a result of altered palatability(e.g., taste, consistency) of different foods.

EXPEEIMENT 2The purpose of the experiment was to de-

termine whether a highly palatable food(chocolate chip cookies) would coax thecontrol rats away from the chow, thus mak-ing their food preferences more similar tothose of the rats with amygdala lesions.

ProcedureThis was the second food selection test ad-

ministered to the rats. The foods and procedurewere the same as for Experiment 1, except thatbroken chocolate chip cookies (Symbol brand"Maryland Cookies") replaced the orange peel.

Results

The three groups of animals ate for simi-lar lengths of time (controls for 252 ± 16sec., Am for 298 ± 18 sec., BL for 304 ± 34sec.). These times do not differ significantly.

The food preferences of the three groupsare shown in Figure 4. The Am group ateless chow than the controls (p < .001) andmore cookies (p < .01). The BL group ateless chow (p < .001) and more cookies (p <.001) than the controls. Other differenceswere not significant. These altered foodpreferences were more extreme in the BLthan the Am group (see Figure 4). Theamount of time that the rats spent eatingcookies indicates that the rats found thempalatable. For example, the BL group atethem for 58% of their total eating time, and

by the sixth food test (see Figure 6) controlrats ate cookies for as much as 32% of theireating time.

Discussion

It can be concluded that the rats withlesions in the amygdala, particularly in thebasolateral region, found the cookies verypalatable and ate little chow. Although thecontrols sampled them, the cookies did notcoax the controls away from eating pri-marily chow.

The difference between the amygdala-lesioned rats and the controls may have beenthat the controls are checked by unfamiliarfood; they would not eat significant quan-tities of an unfamiliar food in unfamiliarsurroundings even if it was very palatable.The amygdala-lesioned rats may not havebeen checked by unfamiliarity. To test this,in Experiment 3 the control rats were re-tested in the previous two test situations(Experiments 1 and 2) to determine whetherwith familiarity they would eat propor-tionately less chow and more of the otherfoods. It should be recalled that the chowwas very familiar to the rats, as it formedtheir regular diet.

EXPERIMENT 3

The purpose of the experiment was to de-termine whether with repeated testing thefood preferences of the control rats wouldbecome like those of the rats with lesions inthe amygdala.

ProcedureFurther food tests were carried out on 12 of

the control rats. In Tests 3 and 4, for which re-sults are not reported here, the rats were offeredthe same foods as in Experiment 1. Then Tests5 and 6 were administered to the control rats,forming Experiment 3. Test 5 was a repeat ofExperiment 1 (see Figure 1) and Test 6 of Experi-ment 2. Twelve of the rats, chosen randomlyfrom the unoperated control rats of the precedingexperiments, comprised the control group in thepresent experiments.

Results

In Test 5 the control rats ate for 342 ±36 sec. compared with 158 ± 17 sec. for thesame 12 rats in Test 1 (Experiment 1). Thedifference is significant (p < .001). In Test6 the control rats ate for 378 ± 27 sec. com-

FOOD PREFERENCE AFTER AMYGDALA LESIONS

Test 2

70 r

253

enc

Cont (19)Am (33)BL (13)

60

50

40

30

20

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chow cauliflower sultanas potato greens cookies

FIG. 4. Food preferences of the amygdala-lesioned (BL and Am groups) and control rats in Test 2,in which cookies replaced the orange peel of Test 1. (See Figure 3 for further details.)

pared with 227 ± 15 sec. for the same 12rats in Test 2 (Experiment 2). The differ-ence is significant (p < .001). Thus, withfamiliarity, the control rats ate for longerin the test situation. The food preferences ofthis control group of rats in Test 5 areshown in Figure 5. For comparison, thepreferences of these same 12 control rats inTest 1 are shown in Figure 5. It is clear thatthe rats were eating relatively less chowthan in Test 1 (43.7 ± 12.2% vs. 58.8 ±6.8%) and were thus performing more likethe Am group in Experiment 1 (34.4 ±5.4%). The other main food which the con-trol rats now ate was cauliflower (Figure 5;41.9 ± 12.4% vs. 14.2 ± 2.3% in Test 1).

The food preferences of this control groupof rats in Test 6 are shown in Figure 6. Forcomparison, the preferences of these same12 control rats in Test 2 are shown in Figure6. The rats ate less chow than in Experiment2 (23.1 ± 7.7% vs. 44.5 ± 5.3%; p < .05)

and were thus performing more like the Amgroup in Experiment 2 (19.2 ± 4.8%). Themain foods which control rats now ate werecookies (32.1 ± 8.4% vs. 12.2 ± 4.8% inExperiment 2), and cauliflower (30.1 ±7.7% vs. 16.7 ± 4.3% in Experiment 2;Figure 6).

DiscussionIn the repeated tests (5 and 6), when

both the testing situation and the availablefoods were familiar to the rats, the controlrats showed food preferences which weresimilar to those of the rats with amygdalalesions when they were first tested. Thus, theeffect of amygdala lesions in this testingsituation was to allow the animals to eatunfamiliar palatable foods in an unfamiliarsituation. The purpose of Experiments 4 and5 was to determine whether the intact ratswere reacting to unfamiliarity of the foodsor unfamiliarity of the testing situation.

254 EDMUND T. -ROLLS AND BARBARA J. ROLLS

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60 . Io, 50E*•*

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a test 5

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^ fh fi, ^FIG. 5. Food preferences of 12 control rats in Test 5, in which the foods were the same as those avail-

able in Test 1. (For comparison, the food preferences of the same 12 control rats in Test 1 are shown inthe unshaded histogram. See Figure 3 for further details.)

EXPERIMENT 4

A number of new foods were given to theanimals in the familiar testing situation.The purpose of the experiment was to de-termine whether unfamiliar foods would besufficient to make intact control rats againeat a large proportion of their familiar chowcompared to the amygdala-lesioned rats.

Procedure

The test cage and procedure were as describedfor the earlier tests. The foods were standardchow and sultanas and the following unfamiliarfoods, arranged as shown in the inset to Figure7: tomato, banana, mushroom, and carrot. Thesenew foods were fresh, uncooked, and chopped intosmall portions with a maximum dimension of .5cm. There were 12 of the original 19 controls re-maining in the control group, and 11 animals inthe amygdala-lesioned group. Six of the 11 amyg-dala-lesioned animals were from the BL group. Allthe rats had been tested at least four times inthe test cage, so that the test cage and procedurewere familiar to the animals.

Results

The amygdala-lesioned and control groupsof animals ate for similar lengths of time(247 ± 26 sec. and 288 ± 20 sec., respec-tively) . These times are not significantlydifferent.

The food preferences of the groups areshown in Figure 7. The amygdala-lesionedanimals ate much less chow than the con-trols (16.7 ± 3.4% and 45.7 ± 8.3%, respec-tively; p < .01). Thus, an unfamiliar selec-tion of foods was sufficient to make thecontrol rats spend a greater percentage oftime eating chow than the lesioned rats. Theamygdala-lesioned animals sampled and atethe new foods, and ate significantly moremushrooms than the controls (28.1 ± 5.3%and 8.0 ± 4.0%, respectively; p < .01).

Discussion

It can be concluded that intact rats sam-ple unfamiliar foods, but eat only a small

FOOD PREFERENCE AFTER AMYGDALA LESIONS

50r i

O)c

is&"ffl

AO

30

20

10

EH test 2

EH test6

I 1chow cauliflower sultanas potato greens cookies

FIG. 6. Food preferences of 12 control rats in Test 6, in which the foods were the same as those avail-able in Test 2. (For comparison, the food preferences of the same 12 control rats in Test 2 are shown inthe unshaded histogram. See Figure 3 for further details.)

amount on first exposure, while rats withamygdala lesions both sample new foods andeat them immediately if they are palatable.Presenting the control rats with a selectionof unfamiliar foods was sufficient to makethem eat their familiar chow for a high pro-portion (45.7%) of the time, relative to thelesioned animals. The familiarity or unfa-miliarity of the situation in which the foodwas found did not appear to be importantin determining whether the rats would eatfamiliar rather than unfamiliar foods (seeGeneral Discussion section).

EXPERIMENT 5The purpose of this experiment was to

determine whether unfamiliarity with thetest situation, which could lead to fear, is asignificant factor in making intact animalseat familiar chow rather than relatively un-familiar foods. If fear due to the test situa-tion were a significant factor this could be away in which the amygdala-lesioned ratsdiffered from the controls. It has been shownalready in Experiments 1-4 that the majorfactor in determining the preferences of theintact animals is familiarity/novelty of pal-atable foods and that the amygdala-lesionedanimals will eat novel foods.

Procedure

Experiment 1 was repeated on control andlesioned rats twice more, with and without dis-turbing environmental stimuli to make the testsituation unfamiliar and to induce fear. Thenormal and noxious environmental conditions wererun in a counterbalanced experimental design,with at least 2 days between tests for each ani-mal. The environment was made disturbing byplaying a tape recording of loud irregular soundsthroughout each 10-min. test and by concurrentlymaking sudden movements which the rat couldsee in the well-lit test room. The standard taperecording had been made by banging the mi-crophone during the recording. The sudden dis-tracting movements were made by the experi-menter's arms, which did not come closer than1 m. to the test cage. The subjects were 10 ofthe amygdala-lesioned rats and five of the con-trols, run blindly by the experimenter.

ResultsAlthough the disturbances reduced the

total eating times of control (192 ± 37 sec.vs. 254 ± 39 sec.) and amygdala-lesionedrats (213 ± 27 sec. vs. 237 ± 26 sec.), thesedifferences were not significant. The disturb-ances also delayed the times to the onset ofeating. These were 151 ± 62 sec. vs. 84 ± 27sec. for the controls and 158 ± 29 sec. vs. 89±11 sec. for the amygdala-lesioned rats.This effect of the disturbances on the le-

256 EDMUND T. ROLLS AND BARBARA J. ROLLS

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111I1\\chow tomato banana sultanas mushroom carrot

FIG. 7. Food preferences of amygdala-lesioned (Am) and control rats in Experiment 4, in which fournew foods (tomato, banana, mushroom, and carrot) were introduced. (The inset shows the arrangementof the foods. See Figure 3 for further details.)

sioned group was significant (p < .05). It isthus clear that the presence of the noise andmovements did affect the animals' behavior.

The food preferences of the four groupsare shown in Figure 8. It is clear that thepresence of the disturbances had no signifi-cant effects on the food preferences of theanimals.

DiscussionIt is concluded that fear induced by an

unfamiliar and disturbing environment wasnot sufficient in the test situation to alterthe rats' preference for foods.

Additional evidence is provided in Figure8 about the effects of unfamiliarity/noveltyof the foods. All the rats had been giventests with foods similar to these previously(see previous experiments). With this highdegree of familiarity, the preferences of thecontrol rats had become very similar tothose of the rats with amygdala lesions, themain remaining differences being in chowand sultanas.

GENERAL DISCUSSIONIn this study rats with lesions in the

amygdala did not have major defects in the

control of the amount of food they ate. Forexample, their body weights increased asrapidly as those of the intact rats. Further,in the 10-min. food-selection tests used inthese experiments, there were never any sig-nificant differences in the amounts of timethe control and lesioned groups ate in anyone test. This finding is in agreement withthat of other workers, who have failed tofind that amygdala lesions in rats alter bodyweight regulation in a way comparable withthe changes following hypothalamic dam-age (Grossman & Grossman, 1963). Indogs, changes in body weight regulation fol-low amygdala lesions, but these changes alsoare not as large as those which follow hypo-thalamic damage (Fonberg, 1969). It is ofinterest that in the dog, the critical region ofthe amygdala which when lesioned leads toaphagia and then hypophagia is localized inthe region of the central and medial nuclei(Fonberg, 1969, p. 347). This correspondsclosely with the area in which a lesion leadsto aphagia in the rat (see Figure 2).

By testing for food preferences, a majorchange in the ingestive behavior of theamygdala-lesioned rats was found (Experi-

FOOD PREFERENCE AFTER AMYGDALA LESIONS 257

60r

50

~ 40enc

2 30

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CH ContE3 Cont , noise

til Am, noise

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chow cauliflower sultanas potato greens orange peel

FIG. 8. Food preferences of 10 amygdala-lesioned (Am) and 5 control rats in Experiment 5, in whichnoises and movements (noise) were introduced in one of two preference tests received by each rat.(See Figure 3 for further details.)

ments 1 and 2). The lesioned rats sampledand ate new palatable foods, in contrast tothe intact rats, which sampled the newfoods but ate mainly the standard chowwhich formed their normal diet. The reasonthat the control rats preferred chow was notthat they found the new foods unpalatable.After repeated testing had familiarized thecontrols with the new foods, they switchedto preferring some of the new foods. Theirpreferences thus became similar to theamygdala-lesioned rats' preferences (Ex-periment 3 and also 5). Lack of familiaritywith the new foods, rather than with thetesting situation, is the important factor;when unfamiliar foods were introduced intothe familiar testing situation, the controlrats ate much more chow than the amyg-dala-lesioned rats, which ate the palatablenew foods (Experiment 4). This conclusionis supported by the rinding that altering thetesting situation was not sufficient to alterthe food preferences of the rats (Experiment

5). Further, any general factor such as fearin the testing situation was not importantenough to cause differences in the eatingtimes among the groups of animals in anyone experiment. It is concluded that theamygdala-lesioned rats do not have the nor-mal control which prevents rats' eating largequantities of new palatable foods. It ap-pears that in this way the amygdala is in-volved in the selection of foods eaten.

The rats with amygdala lesions did noteat foods indiscriminately. In every experi-ment it was found that the lesioned ratsshowed marked differences in the time spenteating the different foods. These time differ-ences probably represent preferences andaversions, because all the foods were sam-pled. Thus, a change in reward value interms of the palatability of the differentfoods was not a major alteration producedby the lesions; rather, the reward valuecomputed with the aid of previous experi-ence appears to be the aspect of ingestive

253 EDMUND T. ROLLS AND BARBARA J. ROLLS

"Jbehavior altered by the lesions. This pre-vious experience could be of many differenttypes—for example, that which is involvedin "neophobia" (Barnett, 1958; Galef, 1970;Richter, 1953; Rozin, 1968; Shorten, 1954;Weiskrantz & Cowey, 1963) or in learnedaversion (Galef & Clark, 1971; Garcia &Koelling, 1967; Nachman, 1963). Learnedaversion was certainly impaired in theseamygdala-lesioned rats (see following arti-cle).

The basolateral region of the amygdalaappears to be important in the altered foodselection. In Experiments 1 and 2, the BLgroup (13 rats with bilateral lesions in thebasolateral region of the amygdala) showedthe altered food preferences more markedlythan the Am group (i.e., rats with bilaterallesions in the lateral amygdala/pyriformcortex region; this group included the BLrats). This finding provides strong corrobo-rative evidence for the suggestion that thebasolateral region of the amygdala is in-volved in ingestive behavior (E. T. Rolls,1972, 1973). This suggestion was based onthe following series of experiments. First,neurons in the basolateral amygdala areactivated in eating elicited by electricalstimulation of the lateral hypothalamus (E.T. Rolls, 1972). Second, these neurons haveabsolute refractory periods similar to thoseinvolved in the stimulus-bound eating (E. T.Rolls, 1973). Third, the injection of a localanesthetic bilaterally into the amygdalablocks stimulus-bound eating (P. H. Kelly,manuscript in preparation).

These results taken together suggest thatstimulus-bound eating may arise whenamygdaloid neurons normally involved inthe control of ingestive behavior are acti-vated, simultaneous activation of brainstemneurons also being important (see B. J.Rolls & E. T. Rolls, 1973; E. T. Rolls, 1972).The amygdaloid neurons may normally beinvolved in the selection of ingested foods onthe basis of previous experience (Experi-ments 1-5) and therefore when foods arerewarding. Excitation of these neurons instimulua-bound, eating., may therefore makefood in the cage rewarding and lead to eat-ing. This may explain some peculiar char-acteristics of stimulus-bound eating (Val-

enstein, Cox, & Kakolewski, 1970)—forexample, the degree of specificity of thedifferent substances which may be ingestedin stimulus-bound motivational behavior.

Altered feeding behavior has previouslybeen found to follow lesions or stimulationof the amygdala in the rat. Electrical stimu-lation of the "cortico-medial-pyriform tran-sition zone" of the amygdala suppressedfood intake in deprived rats (White &Fisher, 1969). Lesions of the corticomedialamygdala increased the latency to the onsetof eating in a novel environment (Sclafani,Belluzzi, & Grossman, 1970). As the cortico-medial region of the amygdala was involvedin the experiments, the results can not bedirectly compared with the present findings.In experiments on the ventral amygdala, ithas been found that in deprived rats adre-nergic stimuation of the ventral amygdalaproduces an increase in food intake and adecrease in water intake. In deprived rats,cholinergic stimulation of the same site in-creased water intake and reduced food in-take (S. P. Grossman, 1964). The aim of thepresent experiments was to examine changesin ingestive behavior following destructionof the basolateral region of the amygdala,the region found to be activated in stimulus-bound eating and drinking (E. T. Rolls,1972).

Altered food preferences follow lesions ofthe amygdala in monkeys. Following thelesions, the monkeys will accept meat (Ur-sin, Rosvold, & Vest, 1969) and will acceptstrong saccharine solutions (Weiskrantz,1960). Monkeys after bilateral temporallobectomy, which involved the amygdalabut also many other structures, showed re-peated oral investigation of inedible objects(Kliiver & Bucy, 1939). The extent to whichthese changes are dependent on altered con-trol of ingestive behavior by previous ex-perience, as appears to be the case in therat, is unknown.

The altered ingestive behavior of theamygdala-lesioned rats was brought outwell in the 10-inrn.^ood-preference experi-ments described. TheHest situation was alsoeffective in showing that the-^ffects of amyg-dala lesions were not due to'interruption of

FOOD PREFERENCE AFTER AMYGDALA LESIONS 259

the olfactory pathways, for olfactomizedrats in the same situation showed very dif-ferent behavior (E. T. Rolls & M. Burton,unpublished results, 1971). The olfacto-mized rats ate for very much shorter timesthan control rats but had food preferenceswhich were similar to the control rats.

The present finding that the amygdala in-fluences food intake suggests that functionalconnections exist between the amygdalaand the diencephalic systems which controlfeeding. This suggestion is consistent withthe discussion above on the function of theamygdalo-hypothalamic connections. Therole of the amygdala in ingestive behaviorin general is discussed at the end of the fol-lowing paper.

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(Received May 1, 1972)