Physiology & Behavior, Vol. 20, pp. 523--531. Pergamon Press and Brain Research Publ., 1978. Printed in the U.S.A

Predatory Versus Alimentary Behavior after Amygdala Lesions in Cats JOLANTA Z A G R O D Z K A AND ELZBIETA FONBERG

Department o f Neurophysiology, Nencki Institute o f Experimental Biology Pasteura 3, 02-093 Warsaw, Poland (Received 31 May 1977) ZAGRODZKA, J. AND E. FONBERG. Predatory versus alimentary behavior after amygdala lesions in cats. PHYSIOL. BEHAV. 20(5) 523-531, 1978. - In cats the effort of small amygdala lesions on mouse-killingbehavior and food intake was studied. After ventromediai amygdala lesions predatory behavior was abolished for several weeks whereas food intake was only slightly diminished. Lesions of dorsolateral amygdala did not impair the effective predatory behavior, but produced a decrease of food intake. It is supposed that within the amygdala in cats there exist separate regions connected with food getting, i.e., predatory behavior (ventromedial part of amygdala) and food intake from the bowl (dorsolateral part of arnygdala). Motivational basis of the predatory behavior and its relations with aggressive and alimentary mechanisms are discussed. Amygdala lesions

Mousekilling

Predatory behavior

Food intake

different species, the behavioral differences among species were obvious, and the suggestions of authors are convincing and stimulating. Only few authors reported the effects of small, circumscribed lesions of amygdala on alimentary behavior. Collier and Gault [5] and Sclafani et al. [39] observed aphagia after lesions of corticomedial part of amygdala in rats. Grossman and Grossman [17] reported adipsia after small anteromedial lesions in rats. Korczyfiski and Fonberg [25] observed deficits in food and water intake and instrumental performance reinforced by water and solid food after medial amygdalar lesions. Recently Box and Mogenson [4] also observed aphagia after dorsomedial amygdalar damage in rats. The data obtained on cats with small amygdalar lesions are even more scarce. Lewifiska [26] reported short lasting aphagia with subsequent hypophagia after lesions of corticomedial part of amygdala. Other authors observed either aphagia and hypophagia or hyperphagia after large lesions of the amagdala often involving the whole amygdaloid complex [6, 16, 23, 24, 291. As the results of all the previous studies did not give us the clear answer as to whether the role of amygdala is similar in dogs and cats, it seemed interesting to study in more detail the effect of lesions of amygdala in the alimentary mechanisms in cats. In addition, it was interesting to investigate the more specific effects of amygdala lesions on different aspects of the alimentary behavior of cats, taking into account their ethological characteristics as carnivores which in natural conditions get food by means of attacking and killing the prey. Assuming that predatory behavior in cats is primarily

ALIMENTARY mechanisms are complex and involve different sensory, motor, motivational, emotional and metabolic components governed by various brain structures. Most of the authors accept the dominating role of the hypothalamus in feeding. O n the other hand, studies performed on dogs by Fonberg have shown the important role of the amygdaloid complex in the regulation of both inhibitory and excitatory alimentary mechaniams, comparable to that of hypothalamus [10,11]. These experiments demonstrated that lesions of the dorsomedial part of amygdala produce aphagia with long lasting hypophagia and hypodipsia as well as decrease of instrumental performance reinforced by food and impairment of other asepcts of the alimentary behavior [8, 9, 10, 11, 12]. On the other hand, the experiments of various authors performed on species other than the dog furnished different and often controversial results. This controversy was partly caused by the fact that the localization and dimensions of lesions performed by various authors different from each other and might involve antagonistic systems of amgydala [ 10,11 ]. Only a few authors reported the effect of small amygdalar lesions limited to certain nuclei or definite parts of the amygdaloid complex. The other cause of the discrepancy of results obtained by various authors might be produced by species differences. Schwartz and Kling [38], Kling [23] and Kling et al. [24] reported that lesions of the amgydala produced different results on feeding in rats, cats and monkeys. In spite of the fact that lesions performed by these authors were large and often exceeded the amygdaloid complex, involving the surrounding structures, and were moreover not exactly comparable in

'This work was supported by Grant: 10.4.1.01.4.2. of the Polish Academy of Sciences. 2The authors wish to thank Dr. Afelt, Dr. Korda and Dr. Kosmal for their valuable suggestions and Mrs. Raurowicz and Mrs. Krakowska for their technical assistance. 523

524

ZAGRODZKA AND FONBERG

connected with f o o d p r o c u r e m e n t , it may be considered as a particular example of the alimentary behavior. In this paper, which is the part of more extensive studies on the role of the amygdaloid c o m p l e x in cats, we investigated the effect of small amygdalar lesions on the predatory behavior, i.e., food p r o c u r e m e n t in comparison with food acquisition. We compared the food intake of regular laboratory f o o d presented in a bowl, and the eating o f a mouse which first had to be caught and killed by the cat. METHOD Experiments were p e r f o r m e d on 26 naive, adult male cats ( 1 . 5 - 3 year old) weighing 3 . 5 - 6 . 0 kg.

Pretest Before the experimental procedure started, all cats were tested in order to determine their predatory abilities. A live mouse was presented to each cat during a 30 min session in a r o o m 180 × 180 cm. This procedure was repeated three times. If the cat did n o t attack the mouse during all three sessions, it was discarded as nonkiller. In the results o f the pretest nine cats were discarded, i.e., the following experiments were p e r f o r m e d on 17 cats.

Observations of Predatory Behavior Each cat was placed in the test c o m p a r t m e n t . After 5 min the freely moving white mouse was introduced. Every response of the cats to the mouse was observed, as well as other aspects o f his behavior. The latency of the first a t t e m p t of the cat to attack the mouse was registered. The n u m b e r o f occurrences of these attempts, n u m b e r and latency of the effective (muricide) attacks, latency of the onset of eating the mouse and the duration o f c o n s u m p t i o n were also noted. Observations on the cat-mouse interaction were p e r f o r m e d in normal cats before the damage of the amygdala, three times in each of the following situations: (a) the cat deprived of food for 4 2 - 4 4 hr; ( b ) t h e cat food deprived during 1 8 - 2 0 hr for mouse-meat perference test in which fresh meat in the food bowl was presented when the cat was consuming the mouse or just after its killing before he started to eat it; (c) the cat fed ad lib with raw meat immediately before the experimental sessions. After the operation of the amygdala the observations o f the predatory behavior started beginning the third postoperative day. The experimental sessions were p e r f o r m e d twice a week. Therefore, the postoperative investigations involved the period of time after the third day until the fifth week after the surgery. The occasional observations were performed until a p p r o x i m a t e l y the end o f the second month.

thesia (40 mg/kg) and in aseptic standard conditions. Wolfram electrodes (dia. 0.5 m m ) insulated by an enamel except for 0.3 m m of the tip were placed according to the coordinates of the atlas o f Jasper [19]. Electrolytic lesions were made by DC anodal current (2.5 m A ) , applied for 2 min. The cathode was inserted in the skin o f the head.

Histological Verification When the experiments were completed, the animals were anesthetized by overdose of Nembutal, perfused with saline and a 10% solution of Formalin. Brain were preserved in 10% Formalin. The frozen sections 50 u thick were made, and each 10th section was stained by Kl/Jver method. Anatomical verification o f the localization and dimensions of lesions was made. RESULTS

Observations of Predatory Behavior: Before Operation A]?er 4 2 - 4 4 hr of food deprivation. In 14 o f the cats the effective attack occurred immediately (Tables 1 and 2). That is, within 1 sec of presentation o f the mouse the cat caught the mouse in his paws and, in a killing grip, broke its neck. Figure la illustrates the normal predatory behavior. Immediately after killing the mouse, the cat began to eat it, although occasionally the cat would first play with the dead mouse. The duration of the time o f eating the prey varied from 34 sec to 3 min. T w o cats were in the habit o f playing with the mouse before killing it. This play lasted for a p p r o x i m a t e l y 640 sec in the case o f cat n u m b e r 163, and a p p r o x i m a t e l y 140 sec for cat n u m b e r 5. These last two cats exhibited the typical signs o f stalking their prey as described by Leyhausen [ 2 7 ] . Food-mouse preference test (18--20 hr o f deprivation). A cat was presented with a bowl of meat, either immediately after killing a mouse or during its consumption. In most cases (in 41 trials o u t of 43) he showed preference for the killed prey, and consumed it, ignoring the food bowl (Fig. la). After ad lib .feeding. T w o well defined types of behavior were most often observed: (a) the cat watched the mouse passively during the first minute o f tile experiment. Sometimes he stretched out the paw toward the mouse if it happened to be near. Gradually he lost the interest in it and settled d o w n to sleep. (b) The cat killed the mouse as soon as it was introduced into the experimental room, and then he was no longer interested in it and lay down, not paying attention to the prey. No cat ever ate the killed mouse in any of the three trials.

After Operation bbod Intake The a m o u n t of food consumed was tested by so called satiation test. Two times daily the cats were fed ad lib. Once a day a b o u t 8 a.m. they obtained raw minced meat and milk and at 2 p.m. meat soup with cereal and vegetables. The a m o u n t of food consumed was measured during a five day period before operation, 10 days just after operation and again during a five day period, starting from fifth week postoperatively.

Surgery The operation

was performed under Nembutal anes-

On the basis of both behavioral and anatomical differences the cats might be divided into two groups: Group 1. In the group of eleven rats the predatory behavior was impaired postoperatively. During the first postoperative week nine cats (Nos. 50, 80, 9 1 , 3 0 2 , 5 , 2 6 9 , 112, 163, 186) did not show the slightest interest in the mouse (Fig. l b). They were in general apathetic and indifferent, spending most of the time lying down, half asleep and did not show any detectable response either to the voice or petting by the experimenter, or to the other environmental stimuli. Thereafter, they started to react to above stimuli, but they were still indifferent to the mouse. Some of them started to observe the mouse passively

PREDATORY BEHAVIOR IN AMYGDALAR CATS

A.

525

B.

C.

FIG. 1. Cat in predatory situation. A. Before operation. B. After ventromedial amygdala lesion. C. After dorsolateral amygdala lesion. Notice lack of interest in the mouse after ventromedial amygdala damage as compared with normal and dorsolateral amygdalar cats. without moving from their characteristic motionless (sphynxlike) position. Two cats (Nos. 92 and 43) showed an inadequate, clumsy attempt to attack the mouse already on the third postoperative day. It consisted in showing an orienting reaction to the mouse, observing it, moving toward it and when the mouse was near, attempts to reach it with lazy, slow, and inadequate movements of the forepaws. The killing grip by the mouth was never observed. These attempts were very soon abandoned and the cats resumed their indifferent and motionless position. The ability to attack the mouse was however not irreversibly abolished (Table 1). All cats gradually started to attack the mouse, but the recovery of the predatory behavior progressed slowly and in different periods of time in the particular cats. In general, first signs of attempts to attack the mouse begin to appear in the second postoperative week. They were similar as in two above described cats. The cats observed the mice, stretched the paws toward them, but if the mice escaped they did not follow them. The attack became effective in nine cats after five postoperative weeks and in two cats (92 and 43) it recovered already after two weeks (Table 1). These last cats reached the preoperative mean latency of effective attack in the third week after the operation. In three cats the attack was completely ineffective during several experimental sessions, but became effective suddenly in the first second of mouse prepresentation. The same short latency of attack

was characteristic for these cats before the operation. In the remaining cats the latency of effective attack was much longer than before operation, but step by step it became shorter and shorter and these cats also reached progressively their preoperative level of performance. The cats were not impaired in their normal s e n s o r y - m o t o r coordinations, but all their movements were slower and attempts to get the mouse were abandoned with first difficulties. The investigations of motor aria sensory abilities of amygdala cats were the subjects of special studies [1,14]. The longer latency of attack was due to lack of initial interest in the mouse. Some cats directed toward the mice, stretched slowly their paws toward, but they did not show biting attack as it was observed before operation. When the attack reappeared it was always quick and efficient and the killing grip was strong and deadly. The duration of eating the mouse was also changed postoperative. Before the operation the cats devoured the prey during a few minutes without intervals in eating. After the operation, at that period of time when they had already started to eat the mouse, they often interrupted the process of consumption. Cats either left the half-devoured mouse and remained near by, looking around, or went away and came back after a while to continue eating. This kind of behavior greatly prolonged the duration of total consumption. Gradually, the consumption of mouse became faster and interruptions were shorter, reaching the preoperative level after a few weeks.

526

ZAGRODZKA

TABLE

AND FONBERG

1

MEAN LATENCY OF EFFECTIVE A T T A C K IN SECONDS DURING EACH EXPERIMENTAL SESSION

Sessions Before Operation Cat

I

2

Sessions After Operation

3

1

2

3

4

5

6

7

10

8

50

1

1

1

.

.

.

.

*

-*

1

1

1

5

90

180

150

.

.

.

.

*

-*

180

90

120

302

1

1

I

.

.

.

.

.

*

-*

-*

420

1

1

91

1

1

1

.

.

.

.

.

*

-*

-*

-*

1

1

163

540

720

600

.

.

.

.

*

-*

1080

600

600

570

540

80

1

1

1

.

.

.

.

*

300

180

1

1

1

186

1

1

1

.

.

.

.

*

1

1

1

1

1

269

1

1

1

.

.

120

1

1

112

1

I

1

.

.

1

1

92

1

1

1

-*

-*

-*

30

1

43

1

1

1

-*

-*

900

120

10

. .

.

.

*

.

*

-*

-*

-*

-*

480

1

1

1

1

1

1

1

Numbers in the upper row indicate successive sessions, performed twice a week. First postoperative session - on third postoperative day. * A t t e m p t s o f attack, i.e., interest in the mouse. TABLE 2 MEAN LATENCY OF EFFECTIVE A T T A C K IN SECONDS DURING EACH EXPERIMENTAL SESSION

Sessions Before Operation

Sessions After Operation

Cat

1

2

3

1

2

116

1

1

1

90

1

211

1

1

1

1020

207

1

1

1

136

1

1

209

1

!

4

5

6

7

8

9

10

1

1

1

1

1

1

1

I

1

1

I

1

1

1

1

1

I

110

10

15

1

1

1

1

1

1

1

1

70

60

15

5

1

1

1

1

1

1

1

160

I

1

Group 2. In t h e g r o u p o f 5 c a t s ( N o s . 1 1 6 , 1 3 6 , 2 0 7 , 209, 211) an effective predatory behavior was observed i m m e d i a t e l y a f t e r t h e o p e r a t i o n (Fig. I c). H o w e v e r , in t h e first p o s t o p e r a t i v e d a y s , l a t e n c y w a s l o n g e r t h a n b e f o r e o p e r a t i o n ( T a b l e 2). T h e t i m e b e t w e e n m o u s e p r e s e n t a t i o n a n d k i l l i n g grip w a s u s e d as a m e a s u r e f o r a t t e m p t s t o c a t c h t h e p r e y b e c a u s e t h e s e c a t s w e r e less e f f i c i e n t t h a n b e f o r e o p e r a t i o n . All t h e s e c a t s w e r e n o r m a l l y r e a c t i v e , t h e y w e r e v e r y i n t e r e s t e d in t h e m o u s e , e.g., a f t e r e n t e r i n g t h e r o o m , t h r e e o f t h e m at o n c e (as it w a s t h e i r h a b i t p r i o r t o t h e operation) approached the window through which the

3

m o u s e w a s s u p p l i e d . In t h e first p e r i o d a f t e r t h e o p e r a t i o n , all t h e s e c a t s s h o w e d s o m e d e c r e a s e o f m o t o r e f f i c i e n c y . Nevertheless, no neurological distrubances have been obs e r v e d ( Z a g r o d z k a a n d F o n b e r g , in p r e p a r a t i o n ) . In t h e first days after the operation the cats seemed to have some d i f f i c u l t i e s in d e v o u r i n g t h e p r e y . T h e i r j a w m o v e m e n t s s e e m e d t o be s l o w e r a n d as a r e s u l t , t h e t i m e o f c o n s u m p t i o n w a s p r o l o n g e d . T h e m o s t p r o n o u n c e d disturbances were observed when the cats were allowed to h u n t in c o m p e t i t i o n w i t h t h e o t h e r c a t s [ 13 ].

PREDATORY BEHAVIOR IN AMYGDALAR CATS

527

[

•

I ~

l

LArt~

/to

J x

FIG. 2. The effect of ventromedial amygdala lesions on food intake in cats.

Food Intake

In the first postoperative period of 5 days all cats were hypophagic. The cats of Group I (Nos. 50, 80, 91,302, 5, 169, 112, 163, 186, 92, 43) hesitated before starting to eat, and the food intake was slow and without appetite. The decrease of food intake was about 1 2 % - 6 0 % of preoperative level. However on the fourth day most of the

FIG. 3. The effect of dorsolateral amygdala lesions on food intake in cats.

Food-Mouse Preference Test During the first few days after the operation, the cats of Group 1 (Nos. 50, 80, 91, 302, 5 , 2 6 9 , 9 2 , 1 1 2 , 163,186, 43) had been eating the meat spontaneously not paying the slightest attention to the mouse (Fig. lb). Even if the mouse was put into the bowl, on the meat, they consumed the meat, ignoring the mouse. Later, when the predatory behavior was restored, the preference for the mouse was never so consistent as before operation. The cats in some trials preferred meat in the others, mouse. Nevertheless, in 21 out of 33 trials the preference was for the killed prey. However, when these cats started to eat the mouse, they often interrupted its consumption, leaving the mouse half-devoured and starting to eat the meat. Such fluctuations and irregularity lasted till the end of observations, about 2 months. In Group 2 (Cats 1 1 6 , 1 3 6 , 2 0 7 , 2 0 9 , 211), meat-mouse preference was unchanged postoperatively (Fig. 1c). One of the cats, which preferred meat before operation, postoperatively chose meat too.

above enumerated cats started to eat avidly and in the next period of 6 - 1 0 days some of them even surpassed the preoperative level of food consumption. After one month food intake in all these 11 cats was restored to the preoperative level (Fig. 2). Mean values for the whole Group 1 were 42.4 - before operation, 29.5 - during first 5 postoperative days, 39.8 in the next 5 days, and 43.1 during a 5 day period one month later. Standard deviations were respectively: 14.5, 12.1, 7.9 and 14.3. Cats of Group 2 (Nos. 116, 136, 207, 209, 211) were also hypophagic but hypophagia was more pronounced than in the previous group and lasted longer, i.e., during at least 10 days of postoperative observations. Decrease in food intake was about 34% to 60% of preoperative level in the first 5 days, and in the next period of 6 - 1 0 days decrease of the amount of food intake was still about 8% to 53%. Although, all these cats ate much less than before the operation they were interested in food and started to eat without any visible hesitation or distaste. After one month food intake in all five cats within this group was restored near to the preoperative level (Fig. 3). For Group 2 mean values of food intake were 63.6 before operation and 32.5 thereafter 41.1 during next 5 days and 57.4 one month later. Standard deviations for these periods were respectively 13.2, 12.6, 4.8, and 8.3. For both groups one dimentional analysis of variance for correlated data showed a statistically significant difference in food intake between periods of time before and after operation (p