Changes in the feeding behavior of rats after amygdala lesions

BEHAVIORAL BIOLOGY, 12, 265-270 (1974), Abstract No. 4137

BRIEF REPORT Changes in the Feeding Behavior of Rats After Amygdala Lesions

SHERWOOD O. COLE 1

Department of Psychology, Rutgers University, Camden, New Jersey 08102

The feeding behavior of amygdala4esioned male rats was compared to that of normal controls and amygdala shams after 0- or 24-hr food deprivation and after 24-hr food and water deprivation. Results demonstrated that food deprivation was essential for a significant reduction in 1-hr feeding after dorsomedial amygdala damage and that combined food and water depriwition exaggerated such differences in feeding without producing a significant concomitant reduction in drinking. Findings were discussed in terms of the possible role of the dorsomedial amygdala in the central regulation of deprivation-induced feeding.

Changes in feeding behavior after amygdala damage are well documented (see review by Kaada, 1972). Destruction of the dorsomedial amygdala sites decreases food consumption (Fonberg, 1966) and destruction of more basolateral sites increases food consumption (Fonberg, 1968). However, the degree of reduction in feeding after bilateral amygdalectomy appears to differ markedly with different species (Kling and Schwartz, 1961). In addition to the general importance of these findings, the decrease in food consumption accompanying dorsomedial amygdala damage in rats may also make it difficult to obtain an appropriate baseline condition for interpreting the effects of anorexic agents on feeding behavior (Cole, 1973). There is some evidence to suggest that changes in feeding behavior after amygdala damage may involve a general alteration in the sensitivity or responsiveness of lesioned animals to environmental stimuli (Nauta, 1963). Amygdala lesions have been observed to decrease the sensitivity o f subjects to quinine solution (White, 1971) and to 1This research was supported by a Faculty Fellowship from the Rutgers University Research Council and was conducted while the author was visiting investigator at the Laboratory of Psychobiology and Psychopharmaeology, Rome, Italy, during the academic year 1971-1972. Reprint requests should be sent to: Sherwood O. Cole, Psychology Department, Rutgers University, Camden, New Jersey 08102. 265 Copyright © 1974 by Academic Press, Inc. All rights of reproduction in any form reserved.

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reinforcement contingencies (Schwartzbaum, 1960) and increase the sensitivity of subjects to the context within which feeding takes place (Sclafani et al., 1970). Rather than the amygdala serving a primary function in the central regulation of feeding, it probably "modulates" the more basic regulation of feeding by hypothalamic sites through fiber systems (e.g., stria terminalis) connecting the two sites (Grossman, 1964; Sclafani, et al., 1970). The present study was undertaken to investigate further the changes in the feeding of rats after dorsomedial amygdala damage in terms of two basic issues: (1) the dependency of such changes upon food deprivation; and (2) the degree to which such changes are further altered by food and water deprivation, rather than food deprivation alone. Thirty-six 120-day-old male rats of the Charles River strain, weighing 350-450 g, served as subjects. Animals were housed in individual plastic cages in a temperature-controlled laboratory under a regular 12-hr light-12-hr dark schedule and had continuous access to Purina Laboratory Chow and water, except when being tested. Initially, animals were assigned randomly to surgical conditions (normalcontrol, amygdala-sham, amygdala-lesion) to form three groups of 12 rats each. Statistical analysis of body weights demonstrated no difference between groups due to assignment. In the amygdala-lesion group, bilateral electrolytic lesions were produced stereotaxically (2 mA anodal dc current for 20sec) with .25 mm dia monopolar stainless-steel electrodes insulated except at the tip while animals were anesthetized with nembutal sodium (50 mg/kg). A rectal cathode completed the circuit. Flat-skull coordinates for the amygdala (Skinner, 1971) were -0.5 mm posterior to bregma, +4.0 mm lateral to midline, a n d - 8 . 0 mm vertical depth. Surgical procedure for the amygdala-sham group was identical to the above, except that no current was passed after electrode placement. On Trial 1 (3 weeks postsurgery), the 12 animals in each of the surgical groups were assigned randomly to one of two food-deprivation conditions (0or 24-hr) to form two subgroups of six rats each. All animals, then, were administered a single 1-hr free-feeding test in the home cage between the hours of 10:00 AM and 2:00 PM. Animals had free access to water during the deprivation period and testing. To begin the test, a ceramic cup containing dry-ground Purina Laboratory Chow was introduced into the cage. Food consumption for the 1-hr period was measured by weighing the cup at the beginning of the test, weighing it again at the end of the test, and taking the difference in weight as amount consumed. Food spillage was collected from a small tray under the cup and an appropriate correction was made in the feeding data. Water consumption also was measured (in milliliters) during the l-hr test period. On Trial 2 (5 wk postsurgery), the 12 animals in each of the surgical groups were all retested after 24-hr food and water deprivation. The pro-

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cedure, hours of testing, and the measurement of food and water consumption were identical to those of Trial 1. After completion of the study, the amygdala-lesion and amygdala-sham animals were sacrificed, perfused with 37% formaldehyde solution, and the brains extracted for frozen sectioning (40/~m) and staining. By the third postsurgery day, the average body weight of the amygdalalesion animals had dropped to approximately 90% of their presurgery level. However, by the eighth postsurgery day, they had regained most of this loss and, relative to the nonlesioned animals, remained quite stable thereafter. Since the mean body weights of the three surgical groups did not differ significantly on either trial, all feeding and drinking data were analyzed without statistical adjustment. On Trial 1, the mean body weights of the arnygdala-lesion, amygdala-sham, and normal-control groups were 425, 435, and 439 g, respectively ( F < 1.00) and on Trial 2, 433, 445, and 443 g, respectively (F < 1.00). The mean amount of food consumption for the three surgical groups during a 1-hr test after 0- or 24-hr food deprivation on Trial 1 is summarized in Table 1. Analysis of these data (see Table 1) demonstrated a significant effect of surgery, a significant effect of deprivation, and a significant surgery X deprivation interaction. Since the food consumption of the three surgical groups did not differ under the 0-hr deprivation condition (F ~ 1.00), it is apparent that the significant surgery X deprivation interaction was due primarily to the difference in the food consumption of the amygdala-lesion group in comparison to the other two groups under the 24-hr deprivation condition. Overall analysis of Trial 1 water consumption data demonstrated no significant effect of surgery or deprivation, and no surgery × deprivation interaction. The mean amount of food and water consumption for the three surgical groups during a 1-hr test after 24-hr food and water deprivation on Trial 2 is summarized in Table 2. Analysis of the food consumption data (see Table 2) TABLE1 Mean Amount of Food Eaten (g) by Noimal-Control (N-C), Amygdala-Sham(A-S), and Amygdala-Lesion(A-L) Groups During a 1-hr Test After 0- or 24-hr Food Deprivation Deprivationa condition

N-C

Groupsb A-S

A-L

0 hr 24 hr

9.17 18.33

10.00 19.67

7.80 10.67

aDepfivation effect (F (1,29) = 51.93, P < 0.01). bSurgery effect (F (2,29) = 11.01, P < 0.01). a X bSurgery × deprivation interaction (F (2,29) = 6.15, P < 0.01).

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TABLE2 Mean Amount of Food (g) and Water (ml) Consumption by Normal-Control (N-C), Amygdala-Sham (A-S), and Amygdala-Lesion (A-L) Groups During a 1-hr Test After 24-hr Food and Water Deprivation Groups Data Source

N-C

A-S

A-L

Fooda consumption (g)

24.33 b

28.83 c

12.27d

Watere consumption (ml)

18.75

18.33

15.00

aSurgery effect (F (2,32) = 25.62, P < 0.01). b - CComparison (F(1,22) = 3.57, P > 0.05). b - dcomparison (F(1,21) = 23.48, P < 0.01). c - dcomparison (F(1,21) = 56.42, P < 0.01). eSurgery effect (F(2,32) = 2.93, P > 0.05). yielded a significant difference between surgical groups. The normal-control and amygdala-sham groups were not significantly different; however, the normalcontrol and amygdala-lesion groups differed significantly as did the amygdalasham and amygdala-lesion groups. Analysis of Trial 2 water-consumption data (see Table 2) yielded no significant difference between surgical groups, although the mean amount of water drunk by the amygdala-lesion group was slightly less than that drunk by the other two groups. Histological examination of the 12 amygdala-lesion brains indicated that all animals sustained bilateral damage to the dorsomedial portion of the amygdala. The damage involved the central nucleus and the adjacent areas in the region of the stria terminalis. A lesion representative of this group is reconstructed in Fig. 1. One of the animals (No. 31) had bilateral damage to cortical sites as well as the amygdala due to electrode tract leakage. Since the brain damage and consumption data for this animal differed markedly from that of other animals in the group, it's scores were deleted from all previous summaries and analyses, with an appropriate adjustment being made in the statistical degrees of freedom. Histological examination of the 12 amygdalasham brains indicated good bilateral placements and that the tips o f the electrode tracts were in the same general dorsomedial region of the amygdala as were the lesions. The results o f the present study are generally consistent with the previously reported findings o f a decrease in feeding after dorsomedial

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AMYGDALA LESIONSAND FEEDING

0,0

-0.5

-I.O

Fig. 1. Reconstruction of dorsomedial amygdala damage representative of that found in the lesion group (Animal 8). Reconstruction is adopted from Skinner (1971). amygdala damage in dogs (Fonberg, 1966) but do suggest the need for qualifying such findings. First, the results of Trial 1 suggest that the reduction in food consumption resulting from dorsomedial amygdala damage is dependent upon some degree of food deprivation. Although the amygdala-lesion group consumed slightly less food than the other two groups after 0-hr food deprivation, it was only after 24-hr food deprivation that the difference in the 1-hr food consumption of the amygdala-lesion group reached statistical significance (see Table 1). Not only is the reduction in feeding after dorsomedial amygdala damage dependent upon the subjects being food deprived, but an increase in feeding resulting from stimulation of amygdala sites also appears to be dependent upon such conditions (Grossman, 1964). Interactions of the present type (surgery × deprivation) need to be identified before one can specify the nature of the feeding changes resulting from dorsomedial amygdala damage. Second, the results of Trial 2 suggest a basic priority principle regarding the role of the dorsomedial amygdala in the regulation of feeding and drinking behavior. The combined effects of 24-hr food and water deprivation under the conditions of the present study merely resulted in an exaggeration of the difference in the feeding data of the amygdala-lesion subjects without producing any significant difference in the water consumption of the surgical groups (see Table 2). Although it is difficult to ascertain the interdependency of feeding and drinking under Trial 2 conditions, the results do suggest that dorsomedial amygdala damage produces a deficit in deprivation-induced

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feeding but not in deprivation-induced drinking. Evidence presented by Grossman (1960, 1964) suggests that, in the amygdala as well as in hypothalamic sites, feeding is an adrenergic system, whereas, drinking is a cholinergic system. Differences in the distribution of adrenergic and cholinergic sites in the amygdala may, very well, be the basis for the selective alterations in the deprivation-induced feeding resulting from dorsomedial amygdala damage in the present study.

REFERENCES Cole, S. O. (1973). Changes in amphetamine anorexia following amygdala lesions in rats. Proceedings 81st. Annual Convention, APA, 1043-1044. Fonberg, E. (1966). Aphagia, produced by destruction of the dorsomedial amygdala in dogs. Bull. Polish Acad. Sci. (Biology), 14, 719-722. Fonberg, E. (1968). The role of the amygdaloid nucleus in animal behavior. Progr. Brain Res. 22, 273-281. Grossman, S. P. (1960). Eating or drinking elicited by direct adrenergic or cholinergic stimulation of the hypothalamus. Science 132, 301-302. Grossman, S. P. (1964).. Behavioral effects of chemical stimulation of the ventral amygdala. J. Comp. Physiol. PsychoL 57, 29-36. Kaada, B. R. (1972). Stimulation and regional ablation of the amygdaloid complex with reference to functional representations. In B. E. Eleftheriou (Ed.) "The Neurobiology of the Amygdala." New York: Plenum Press. Kling, A., and Schwartz, N. B. (1961). Effects of amygdalectomy on feeding in hqfant and adult animals. Fed. Proe. 20, 335. Nauta, W. J. H. (1963). Central nervous organization and the endocrine motor system. In A. V. Nalbandov (Ed.) "Advances in Neuroendocrinology. Urbana: University of Illinois Press. Schwartzbaum, J. S. (1960). Changes in reinforcing properties of stimuli following ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 53, 388-395. Sclafani, A., Belluzzi, J. D., Grossman, S. P. (1970). Effects of lesions in the hypothalamus and amygdala on feeding behavior in the rat. J. Comp. Physiol. Psychol. 72, 394-403. Skinner, J. E. (1971) "Neuroscience: A Laboratory Manual." Philadelphia: Saunders. White, N. (1971). Perseveration by rats with amygdaloid lesions. J. Comp. Physiol. Psychol. 77, 416-426.