Journal of Neuroscience Research 1 :333-341 (1975)

CONSUMMATORY BEHAVIOR AS A FUNCTION OF AMBIENT TEMPERATURE IN SEPTALLESIONED AND CONTROL RATS J. Sanes, P.J. Donovick, and

R.G.Burright

Department of Psychology, State University of New York a t Binghamton

Septa1 lesions or control operations were produced in male and female rats. Measurements of water and food consumption were carrpd out while the rats were housed under warm vivarium temperatures (24 C) and when maintained in a cold room (6OC). Examination of the data from the entire week spent in the cold revealed that rats with septal lesions deviated from precold water-consumption levels less than comparable control rats. Further, whereas rats with septal lesions suppressed intake for the first 24 hr following either shift in environmental temperatures, control animals inhibited drinking only when returned to the warm environment. Both surgical groups elevated food consumption in the cold. The relative amount of food and water consumed during the day (vs night) increased for all groups when maintained in the cold. Differences in degree of reactivity to the manipulations were observed in male and female rats. These findings were interpreted as adding further support to our contention that septal lesions alter the behavioral (rather than direct metabolic) adaptations an animal makes to its environment. Key words: septal lesions, food consumption, water consumption, environmental temperature. cold, diurnal, male and female rats

On the basis of electrophysiological(20) and behavioral data (10, 11) we have proposed that the septal region of the forebrain is one portion of a comparator mechanism involved in the integration of sensory stimulation with need state and past experiential information. This portion of the limbic system has been shown to be important in the rat's ability to cope with changes in the environment. Thus, as recently reviewed by Fried (17), damage to the septal region alters regulatory mechanisms involved in food and water consumption, reactivity to environmental stimuli, and performance in many classical learning situations. Disruption of the comparator mechanism results in overresponding to some classes of stimuli at the expense of others. For instance, following septal lesions rats may refuse to drink unpalatable solutions at the expense of incurring large, at times fatal, water deficits (1, 1 1). Address reprint requests to Peter J . Donovick, Department of Psychology, State University of New York, Binghamton, New York 13901. J. Sanes is now at the Department of Psychology, University of Rochester, Rochester, New York.

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0 1975 Alan R. Liss, Inc., 150 Fifth Avenue, New York, N.Y. 10011

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Circumstantial evidence would suggest that the septal region is important in the behavioral regulation of other basic homeostatic systems as well. For example, the firing rate of septal neurons is affected by ambient temperature (12, 13); rats with septal lesions have core temperatures comparable to control animals in both warm and cold environments (21); and septal lesions have no affect on the rate of heat loss nor on the shivering response in cats exposed t o the cold (27,28). However, septal lesions do change how the organism responds to fluctuations in environmental temperature. For example, rats with septal lesions maintained in the cold, bar press with greater frequency for heat reinforcement than control rats (29), and we have also observed that following a transient elevation in environmental temperature, control rats increased their fluid intake, but those with septal lesions did not(7). Working with normal animals only, Fregly (14, 15) found that rats maintained in the cold for 10 or 20 days increased their food intake but did not elevate fluid intake relative to animals maintained at standard temperatures. But when returned to the original, normal housing temperature conditions (or elevated temperatures) there was an immediate increase in water consumption (2, 16). Since earlier inquiries (23,25,26) indicated a possible differential pattern of reactivity following septal lesions in the two sexes, we investigated the effects of septal lesions in male and female rats on the amounts of food and water consumed under standard housing or cold environmental temperature conditions.

METHOD

Twenty male and 20 female albino Sprague-Dawley derived rats which were approximately 60 days of age were obtained from Taconic Farms; they weighed between 259-328 gm and 183-201 gm, respectively, at the time of surgery. The animals were run in two separate single-sex replications during the fall and winter of 1973. For surgery, like-sexed groups were matched according to intake to bodyweight ratios. Three females died during surgery and 4 females were later discarded from the data analysis on the basis of histological considerations; the final group sizes were: male control, n = 10; male septal, n = 10; female control, n = 7 ; female septal, n = 6 . All rats were individually housed on a transportable rack in a room where the light cycle was 10 hr light (0800-1800 h) and 14 hr dark. Purina Laboratory Rat Chow Pellets and deionized water were available ad libitum. The water, maintained at ambient air temperature during all phases of the study, was presented in a 100 ml capacity Richter tube mounted on the front of each animal's cage. Environmental temperature upon receipt, and continuing through the first 2 weeks post surgery, was maintained at 24°C 2°C; humidity was not controlled during the study. One week post surgery the food pellets were removed from all cages and replaced by factory-ground Purina Lab Chow presented in food cups (Wahman LC-306) psitioned in close proximity to the Richter tubes. Food spillage was minimized by the placement of a scatter disc on the top of the powdered food. In the event of food spillage the debris was collected, weighed, and then discarded. Food and water were replenished daily and the respective receptacles were cleaned when necessary. Immediately subsequent t o the 0800 hr consummatory measurement of day 15 post surgery, the animals were transported to a cold room for a 1 week period. The temperature of the cold room ranged from 6°C to 8 O C . The water and food supply for the cold period was kept within the cold room. At the end of one week cold exposure, again immediately after measurement of consumption at 0800 hr, animals were returned to the original vivarium temperature (24°C f 2°C). Food (ground chow) and water-intake measurement was continued until the +_

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end of week 4 post surgery (seven days post cold); ad libitum food uellets were then reintroduced to the animals. All rats were weighed periodically throughout the experiment. Data Collection and Analysis

Throughout the study, water consumption was measured either once (1800 hr) or twice (0800 and 1800 hr) a day. During weeks 2-4 post surgery, food consumption was measured to the nearest gm. When animals were moved to a new temperature, water intake was recorded every 15 min for the first hour following the change and then hourly for the 4 subsequent hours. The normal evening reading was also recorded on these two days. Individual median intake values of the weekly blocks were computed and were utilized to derive intake to bodyweight ratios. Because of water absorption or evaporation by the food when animals were transported into a new temperature condition, food consumption data was not evaluated on the change days. The bodyweights used to derive daily intake to bodyweight ratios were the means of individual weights measured at the beginning and end of a week. To describe central tendencies group medians were used, with the exception of mean bodyweights. Data were statistically analyzed using two-tailed Mann-Whitney U-tests. Surgery and Histology

Surgical groups were anesthetized with sodium pentobarbital (40 mg/kg) supplemented with local application of lidocaine hydrochloride. Modified Kopf and Baltimore stereotaxic instruments were used to produce the brain damage; the modification consisted of a head holder which horizontally positioned the head without the use of earbars. Bilateral lesions were produced by passing a 1.5 ma anodal current through the uninsulated tip (0.5 mm) of a stainless-steel pin to a rectal cathode for 20 sec. Coordinates for the septal lesions, in mm, were 1.O anterior to bregma, k 2.5 lateral angled 25" toward midline, and 5.5 deep from surface of the cortex. Control animals were subjected t o the same surgical procedure, including drilling of the skull, but the electrode was not lowered into the brain. Subsequent to consummatory testing, animals were anesthetized with a lethal dose of pentobarbital (100 mg/kg) and intracardially perfused with isotonic saline followed by 10% formalin. The brains were removed and fixed in 10% formalin for at least seven days and then coronally sectioned by the frozen tissue technique at 80 micra. Every fifth section was mounted and stained with a metachromatic stain for cell bodies and fiber tracts (4). Microscopic examination of the histological material revealed that the septal lesions were typically large, bilateral, and restricted to the precommissural septum. The smallest lesions spared portions of the lateral nucleus while the largest extended into the posterior septum and destroyed tissue in the fimbrial nucleus. No damage was seen in the corpus callosum or cingulate cortex. In one male and one female there was unilateral damage in the lateral preoptic nucleus. Similar lesions were recently illustrated (3,9, 10). There was no apparent correlation between the size or specific locus of these large lesions and the behavioral changes noted in either male or female rats. RESULTS Growth of Male and Female Animals

At surgery, males weighed about 100 gm more than females: 290.8 gm vs 188.4 gm, respectively. Although male septals continued to gain weight following surgery, their growth

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pattern during the first postsurgical week was somewhat retarded relative to male controls: 313.5 gm vs 328.2 gm, respectively (8). In contrast, female septals (210.8 gm) at a similar time postsurgery did not weigh less than female controls (208.6 gm). In fact, at that time and during the cold, female septals weighed slightly more than female controls. Except for the female septal group, the cold exposure decreased bodyweights of all groups: +0.2 gm (female septal) and -3.2 gm for the other groups combined. At the end of the consummatory measurements ( 5 weeks post surgery), males weighed about 140 gm more than the females: 378.7 gm vs 239.8 gm, respectively. Male Consummatory Behavior

Group median water intake (ml) to 100 gm bodyweight (BW) values for the males are shown in the left upper panel of Fig. 1. Prior to surgery both groups of male rats drank approximately 13.9 m1/100 gm BW per day. Despite the marked increase in median water intake during the first week post surgery, and confirming earlier findings (8), it took approximately two weeks post surgery for the difference in water intake between septal and control male rats to reach statistical significance (U = 21; nl = n2 = 10; p < 0.05). During the week of cold exposure the median daily water intake of septals increased slightly to 14.4 m1/100 gm BW , and controls increased to 14.2 ml/100 gm BW. However, half the animals in the septal group decreased their water consumption when moved t o the cold, whereas all but one of the control animals increased their water intake (change scores: U = 12; nl = n2 = 10; p < 0.02) (however, cf. 14, 15). One week post cold the control rats decreased their water intake to 12.9 ml/l00 gm BW, while the septal males increased to 15.0 m1/100 gm BW. By the second week post cold, septal intake decreased to 13.9 m1/100 gm BW, and the control intake continued to decrease to 12.0 m1/100 gm BW. Considering intake change scores of individuals between the cold week and both weeks post cold, the septal group was virtually unaffected by this temperature alteration, while the median change score of controls was - 1.68 m1/100 gm BW (U = 19; nl = n2 = 10; p = 0.02). Here, every control animal lowered its water consumption, but only 5 of the 10 male rats with septal lesions decreased their intake subsequent to the move from the cold t o the warmer temperature vivarium. Food intake data for the male animals is displayed in the left middle panel of Fig. 1. At no point were there any statistically significant differences in food consumption between surgical groups. Following surgery (prior to cold exposure) both male surgical groups were consuming approximately 8.0 gm/100 gm BW of food. The cold exposure, as expected (14, 15), elevated the food intake of both groups to a group median of about 11.0 gm/100 gm BW. Following exposure to the cold, male rats decreased their food consumption to around 8.5 gm/lOO gm BW. The group patterns of the ratio of food to water consumption (lower left panel of Fig. 1) is a reflection of the changes in males’ water consumption described above for the control and lesioned rats. However, in all temperature conditions, the control group displayed higher food t o water ratios than the septal group. The immediate (24 hr) change in water intake of male rats when moved to different temperature conditions is shown in the left panel of Fig. 2. When transported to the cold room, the male septal rats decreased their water intake, while the control group drank more water than they had on the previous day in the warmer vivarium. Group median water intake difference scores of individuals for this first-day change from warm to cold were - 1.2 ml/100 gm BW for the septals and +1.2 m1/100 gm BW for the control rats ( U =

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Thermogenic Feeding and Septa1 Lesions

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s

~ 2 4 * C 3 6 * 24.C C ~

4

P r r ~ 2

0

4

s

k24*Cd[6*C]k24*C{

-

-WEEKS POST SURGERY [AMBIENT TEMPERATURE]

Fig. 1 . Median daily water intake in ml/lOO gm bodyweight (BW) (upper panels), food intake in gm/lOO gm BW (middle panels), and food/water ratios based upon weekly data blocks for both septal- and control-group males (left panels) and females (right panels). Week 3 post surgery represents the week during which animals were housed in the cold room (6°C).

21 ; nl = n2 = 10;p < 0.05). The difference between the unconnected points for days 15 and 21 reflect the general tendency for increases in daily consumption seen in both surgical groups over the entire week in the cold (6°C). When the rats were returned from the cold to the normal vivarium temperatures, males with septal lesions again decreased their consumption, but in this case, the control animals responded similarly (but cf. 2, 16). Group median water intake difference scores of individuals for this first day of warm to cold transition were -0.7 m1/100 gm BW for septals and -0.7 ml/l00 gm BW for controls. As expected (9,all males consumed more water during the dark than during the light under both warm and cold conditions. During the week prior to cold exposure, the

338

Sanes, Donovick, and Burright MALES

FEMALES

Soptal 0-

0

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Control

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L

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T . 14 [24*C]

T IS 21 F S 0 C 4

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. 14 [24'C]

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DAY POST SURGERY [AMelENT TEMPERATURE] Fig. 2. Median daily water intake in m1/100 gm bodyweight (BW) for both septal- and control-group males (left panel) and females (right panel) on the days immediately preceding and following the move from warm to cold (days 14 and 15 post surgery) and on the days immediately preceding and following the move from cold to warm (days 21 and 22 post surgery). The ordinate is approximately three times larger than the ordinate for the upper panels (water intake) of Fig. 1.

median water consumed during the dark was 13.1 mlf 100 gm BW per day for the septal group, while the controls drank 11.6 m1/100 gm BW over this period (U = 24; nl = n2 = 10; 0.05 < p < 0.10). At this time, water intake during the light did not differ statistically between groups and was approximately 2.5% of the total daily water consumed. Thus, the elevated consumption of the septal rats during normal temperatures was apparently due to higher intakes during the dark. In the cold, both groups still consumed more water in the dark, but the percentage of total consumption during the light increased to 8.9% for the septals and to 10.3%for the control rats. In addition, during the dark period in

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Thermogenic Feeding and Septa1 Lesions

the cold, water intake of the controls increased to 12.6 m1/100 gm BW, whereas the median septal water consumption in the cold remained virtually the same as the precold levels. Return of the animals to warmer environmental temperatures resulted in a reinstatement of diurnal intake patterns similar to those observed prior to the cold exposure. When maintained in the cold, total food consumed during both the light and dark periods increased for both groups. While most of the food was taken in the dark, both groups increased the percentage of total food taken in the light from approximately 8%in the warm vivarium to 18.5%in the cold vivarium. Female Consummatory Behavior

Water consumption of the female rats is displayed in the upper right panel of Fig. 1. Female septals increased their water consumption more than control females during the first 2 weeks post surgery. By the second week, the female septals were consuming 20.6 ml/lOO gm BW, while the controls were drinking 15.0 ml/lOO gm BW (U = 6; nl = 6, nz = 7; p = 0.034). During the cold exposure, the female septal group decreased their water consumption by - 1.2 m1/100 gmBW, but the control female rats increased theirs by +3.0 m1/100 gm BW (change score: U = 3; nl = 6, nz = 7; p = 0.008). When returned to the warmer temperature, the female control group’s water consumption sharply declined to (or below) levels of the precold week. In contrast, the female septal group did not show such a marked change. Thus, the precold septal-control difference was reestablished (U = 8; nl = 6, n2 = 7; p = 0.074). Although both groups of female rats increased food consumption during the cold (right middle panel, Fig. l), there were no statistically significant group differences in the food to BW ratios under either temperature condition. Thus, the food/water ratios shown in the lower right panel of Fig. 1 again reflect the differential patterns of water consumption in septal-lesioned and control rats. The immediate (24 hr) water consumption reaction to shift in housing temperature of female rats is displayed in the right panel of Fig. 2. When transported to the colder temperature, the septal group decreased their water intake while the control females increased theirs. The grout, medians of individual change scores in 24 hr water intake for this warm to cold transition were -3.1 m1/100 gm BW for the septals and +0.5 m1/100 gm BW for the controls (U = 7; nl = 6, n2 = 7; p = 0.052). However, when moved from the cold t o the warm, both the septal and control groups decreased their water consumption. The median of individual change scores in water intake for this immediate cold to warm temperature change was -3.8 ml/lOO gm BW for septals and -6.0 m1/100 gm BW for controls (U =14; not significant). A similar pattern was observed in weekly food consumption, that is, following surgery, females ate about 10.5 gm/100 gm BW, in the cold they ate 13.7 pm/IOO gm BW, and when returned to the warm they consumed 11 gm/lOO gm BW. Prior to cold exposure, females consumed most of their food and water during the dark hours; this general pattern was also observed when the females were transferred to the colder environment. However, both food and water consumption during the light hours increased in both absolute quantity and percentage of total intake when animals were maintained in the cold. Thus, female rats with septal lesions consumed 5.8%of their water during the light prior to cold exposure and increased to 10.8% of total water intake when placed in the cold; the control rats originally consumed 5.4% in the light and increased to 14.2% with this temperature change. Both groups decreased their intake to about 3.4% of total intake in the light when returned to warmer conditions.

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DISCUSS I0N

This data further supports our contention that the septal region is involved in the behavioral, rather than physiological (metabolic), regulation of basic homeostatic mechanisms. As expected (2 1, 27, 29), there was no indication that rats with septal lesions were unable to regulate body temperature in the cold. Thus, changes in reactivity to environmental temperature as reflected in consummatory as well as other behaviors (29) are interpreted as an indication of the role of this structure in determining behavioral responsivity in the face of environmental challenge. It may be critical to distinguish between the immediate and longterm consequences of environmental challenges ( 2 , 3 , 6 , 14, 15, 16). In the present experiment both male and female rats with septal lesions showed an immediate (first 24 hr) decrease in water consumption when transported from a warm vivarium to the cold room. In contrast, control animals did not immediately change their intake as dramatically nor even in the same direction when moved into the cold room, but instead gradually increased their intake over the week to equal or exceed the levels of the septal groups (however, cf. 14, 15). When returned to warmer conditions, rats with septal lesions, regardless of sex, again showed a prompt decline in water consumption. However, under this cold to warm temperature transition, control rats also exhibited an immediate and similar marked decline in water intake (but cf. 2, 16); this change was most striking in the female control group (Fig. 2). Clearly, the effects observed following septal lesions are dependent on the genetic substrate (18,24) and experiential history ( 3 , 6 , 9 , 1 0 , 2 2 ) of the experimental animal. As we have just indicated, critical distinctions must be made between the short- and long-term consequences of such manipulations. Finally, interactions between a variety of experiential and genetic manipulations are to be expected. Thus, although we have suggested (1 1) that the septal region is part of a comparator mechanism important in the integration of behavior, further specification of the septum’s role in such functions will demand ever increasing attention to the specifics of both historic and task variables. That comparator operations are performed by the brain is clear; how the comparator system(s) is organized is still veiled by the shrouds of uncertainty. AC KNOW L EDGM ENTS

We thank Douglas Dorph and Roger Sikorszky for their assistance. This research was supported by NSF Grant B043534 and funds from the State University of New York Research Foundation. REFERENCES 1. Beatty, W.W., and Schwartzbaum, J.S. Enhanced reactivity to quinine and saccharine solutions following septal lesions in the rat. Psychon. Sci. 8:483-484 (1967). 2. Box, B.M., Montis, F., Yeomans, C., and Stevenson, J.A.F. Thermogenic drinking in cold-acclimated rats. Am. J. of Physiol. 225:162-165 (1973). 3. Burright, R.G., Donovick, P.J., and Zuromski, E.S. Septa1 lesions and experiential influences on saline and saccharin preference-aversion functions. Physiol. Behav. 12:95 1-959 (1974). 4. Donovick, P.J. A metachromatic stain for neural tissue. Stain Technology 49:49-51 (1 974). 5. Donovick, P.J., and Burright, R.G. Diurnal drinking of rats with limbic system lesions maintained in an open vivarium. Physiol. Behav. 11:655-660 (1973). 6. Donovick, P.J., Bliss, D.K., Burright, R.G., and Wertheim, L.M. Effect of pinealectomy or septal lesions on intake of unpalatable fluids in rats given sodium deplete or replete diets. Physiol. Behav. 10:1095-1099 (1973).

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7. Donovick, P.J., Burright, R.G., and Gittelson, P.L. The effects of septal lesions on saccharine choice as a function of water deprivation. Physiol. Behav. 3:677-681 (1968). 8. Donovick, P.J., Burright, R.G., and Gittelson, P.L. Bodyweight and food and water consumption in septal lesioned and operated control rats. Psychol. Rep. 25:303-310 (1969). 9. Donovick, P.J., Burright, R.G., and Bentsen, E.O. Presurgical dietary history and behavior of control and septal lesioned rats. Dev. Psychobiol. 8:13-25 (1974). 10. Donovick, P.J., Burright, R.G., and Swidler, M.A. Presurgical rearing environment alters exploration, fluid consumption, and learning of septal lesioned and control rats. Physiol. Behav. 11:543-553 (1973). 11. Donovick, P.J., Burright, R.G., and Zuromski, E. Localization of quinine aversion within the septum, habenula, and interpeduncular nucleus of the rat. J. Comp. Physiol. Psych. 71 :376-383 (1970). 12. Eisenman, J.S. Pyrogen-induced changes in the thermosensitivity of septal and preoptic neurons. Am. J. Physiol. 216:330-334 (1969). 13. Eisenman, J.S., and Jackson, D.C. Thermal response patterns of septal and preoptic neurons in cats. Expl. Neurol. 19:33-45 (1 967). 14. Fregly, M.J. Effects of extremes of temperature on hypertensive rats. Am. J. Physiol. 176:273-281 (1 954). 15. Fregly, M.J. Water and electrolyte exchange in rats exposed to cold. Can. J. Physiol. Pharmac. 4 6 3 7 3 -88 1 ( 1 968). 16. Fregly, M.J., and Waters, I.W. Water intake of rats immediately after exposure to a cold environment. Can. J. Physiol. Pharmac. 44:651-662 (1966): 17. Fried, P.A. Septum and behavior: A review. Psychol. Bull. 78:292-310 (1972). 18. Gonsiorek, J.C., Donovick, P.J., Burright, R.G., and Fuller, J.L. Aggression in low and high brainweight mice. Physiol. Behav. 12:813-818 (1974). 19. Hart, J.S. Rodents. In: “Comparative physiology of Thermoregulation. Vol. 11: Mammals” (G.C. Whittow, ed.). New York: Academic Press, 1971, pp. 1-149. 20. Hayat, A., and Feldman, S. Effects of sensory stimuli on single cell activity in the septum of the cat. Expl. Neurol. 43:298-313 (1974). 21. Heller, A,, Harvey, J.A., Hunt, H.F., and Roth, L.J. Effects of lesions in the septal forebrain of the rat on sleeping time under barbiturate. Science 131:662-664 (1960). 22. Kemble, E.D., Levine, M., Gregoire, K., Loepp, K., and Thomas, T. Reactivity to saccharin and quinine solutions following amygdaloid or septal lesions in rats. Behav. Biol. 7:503-512 (1972). 23. Kondo, C.Y., and Lorens, S.A. Sex differences in the effects of septal lesions. Physiol. Behav. 6:481-485 (1971). 24. Laughlin, M.E., Donovick, P.J., and Burright, R.G. Septal lesions in meadow voles and mongolian gerbils: Consummatory and investigatory behavior. Physiol. Behav. (in press). 25. Lorens, S.A., and Kondo, C.Y. Differences in the consummatory and operant behaviors of male and female septal rats. Physiol. Behav. 6:487-491 (1971). 26. Singh, D., and Meyer, D.R. Eating and drinking by rats with lesions of the septum and the ventromedial hypothalamus. J. Comp. Physiol. Psychol. 65:163-166 (1968). 27. Stuart, D.G., Kawamura, Y., and Hemingway, A. Activation and suppression of shivering during septal and hypothalamic stimulation. Expl. Neurol. 4:485-506 (1961). 28. Stuart, D.G., Kawamura, Y., Hemingway, A., and Price, W.M. Effects of septal and hypbthalamic lesions on shivering. Expl. Neurol. 5:335-347 (1962). 29. Wakeman, K.A., Donovick, P.J., and Burright, R.G. Septal lesions increase bar pressing for heat in animals in the cold. Physiol. Behav. 5:1193-1195 (1970).

Consummatory behavior as a function of ambient temperature in septal-lesioned and control rats.

Septal lesions or control operations were produced in male and female rats. Measurements of water and food consumption were carried out while the rats...
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