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Effects of septal lesions on palatability modulation of schedule-induced polydipsia
Physiology and Behavior, Voi. 9, pp. 663-665, Brain Research Publications Inc., 1972. Printed in U.S.A.
BRIEF COMMUNICATION Effects of Septal Lesions on Palatability Modulation of Schedule-Induced Polydipsia 12 M. J. WAYNER AND I. GREENBERG
Brain Research Laboratory, Syracuse University, 601 University Ave., Syracuse, N. Y. 13210 (Received 3 August 1972) WAYNER M. J. AND I. GREENBERG. Effects of septal lesions on palatability modulation of schedule.induced polydipsla. PHYSIOL. BEHAV. 9(4) 663-665, 1972.-The effects of rehtively large septal lesions on schedule-induced drinking of water, quinine hydroehloride, and saccharin solutions in three rats were determined. Results indicate that septal lesions enhance schedule-induced polydipsia and decrease an apparent palatability related inlu'bitory effect on drinking. The absence of these effects in one control animal with extensive damage in the dorsolateral portion of hypothalamus including the zona incerta and ventral thalamic nucleus suggests that these effects might be specific to the septum. Septum
Palatability
Schedule-induced polydipsia
Drinking
Procedure
SCHEDULE-INDUCED polydipsia has become a well documented phenomenon [5] which appears to be only one of a general class of behaviors which are adjunctive both with respect to physiological imbalance and reinforcement [7]. The fact that these behaviors might depend upon motor control functions of the lateral hypothalamus results in some interesting testable hypotheses. As the septum has been implicated in palatability mediated effects on fluid consumption [1, 3, 4], in the determination of water intake [2], and in the facilitation and inhibition of lateral hypothalamic electrical activity [6], it seems reasonable to assume that septal lesions might have some effect on schedule-induced polydipsia. The purpose of the present experiment was to determine the effects of relatively large septal lesions on schedule-induced drinking of water, quinine hydrochloride and saccharin solutions. Results indicate that s e p t a l l e s i o n s enhance schedule-induced polydipsia and decrease an apparent palatability related inhibitory effect on drinking.
Animals were reduced to 80% of their initial body weight and trained to respond on a FI-I min schedule for food reinforcement according to standard procedures in an LVE test chamber for one hr each day. Reinforcement consisted of 45 mg Noyes food pellets and water which was available in a stainless steel ball tipped drinking spout in the wall adjacent to the food delivery mechanism. Bar presses were recorded by conventional electromechanical equipment. Number of bar presses and water consumed during the test session and water intakes in the home cages and daily weights were measured. Water was present at all times in the home cage. After a bar press rate and schedule-induced polydipsia stabilized over a 10 day period, the water available during the test session was replaced with either a 0.008%, w/v, solution of quinine hydrochloride or a 0.05% o-benzoic sulfimide (saccharin) solution for the next 10 days. The order of presentation of the two solutions was varied for each rat. After 10 days of one or the other solution, it was replaced for two days with water, and then the water was replaced for the next 10 days with the other solution. At the end of this 32 day period, large bilateral septal lesions were produced in three animals by means of a temperature controlled radio frequency device. An attempt was made to
METHOD
Animals Four male Wistar rats, 3 0 0 - 4 0 0 g in weight, were selected and kept in individual living cages.
t This research was supported by NSF Grant GB-18414X and NIMH Grant 15473 and Training Grant MH-06969. 2We wish to acknowledge the help of E. Goodall who made the lesions in Dr. R. J. Carey's laboratory at the Syracuse Veterans Administration Hospital. 663
664
WAYNER AND GRk'.ENBtSR(;
destroy a comparable amount of tissue in tile posterior dorsomedial hypothalamus of a fourth animal which was to serve as a lesion control. On the day following surgery, animals were subjected to the same series of treatments in the same order. At the conclusion of the experiment animals were sacrificed with ether and perfused with 0.9% saline followed by 10% formalin. Brains were excised, frozen, cut serially at 60 u, stained with cresyl violet, and the e x t e n t of damage estimated by microscopic examination.
70-
HOH
QUININE
tHCYelt
SACCHARIN
5040.. . . ~ 0,4) • O~O, Je • O-O •
30-
g-4 O"~,OPRE OP O--OI~DST OP
20100
RESULTS
Results are summarized in Figs. 1 and 2. As all the animals with septal lesions displayed essentially the same effects, only the means for the three animals are presented. The mean fluid intakes for the animals during the test sessions are presented as a function of days in Fig. 1. Each 10 day period is presented serially from left to right. After the second 10 day period, water was returned for two days before the solution was changed for the next 10 days. The preoperative or base line data are indicated by solid circles and are connected by a solid line and the four phases of the experiment are indicated by the vertical bars. The postoperative means for similar treatments are indicated by solid circles connected by a broken line. The mean number of bar presses for the three animals are presented in a similar way in Fig. 2. The schedule-induced polydipsia during the first 10 days of the experiment remained relatively constant. Number of bar presses was also relatively stable during this period. When the water (HOH) was replaced with the quinine solution, schedule-induced polydipsia decreased and bar presses increased. When water was returned for two days, the polydipsia increased to the previous level and bar presses decreased. Saccharin produced an immediate and gradual increase in fluid consumption and a precipitous decrease in the number of bar presses. The same general effects were observed following the production of septal lesions except that the magnitude of the differences produced by the quinine and saccharin on fluid intake were attenuated and enhanced by saccharin on the number of bar presses for the last three days. Because of the small number of animals and the sequential nature of the data, only t-tests for correlated samples were calculated for each rat in an attempt to provide some measure of the reliability of the observations. The septal lesions produced a significant increase in the schedule-induced drinking of water in all three animals. The increase postoperatively cannot be attributed to the apparent carry-over of the increase which occurred with saccharin because the order of presentation was different for some animals. Quinine consumption decreased less following the lesions but decreased significantly for the three rats. The consumption of saccharin increased significantly following the lesions. Animals with septal lesions also pressed the bar more when water was available; the t-tests for all animals were significant. When quinine was presented the differences in number of bar presses was also significant. The two pronounced decreases in bar presses which occurred during the presentation of saccharin following the lesions are very obvious and were not associated with a decrease in fluid intake. The decrease was due primarily to decreases in consumption by two of the three animals.
i
60-
I
r
I
I
r
F
5
I0
5
10
5
10
DAYS
FIG. 1. Mean fluid intakes for the three animals during each of the four phases, water, quinine, water, saccharin, as indicated by the vertical lines are presented before and after septal lesions. 9O0
HOH
I
QUININ|
IHOI4[
SACCHARIN
II00 O-
- 0 I~ST OP
700
r,
P, A
o, 2, l~'*'°'°°'g'
6OO
i 1
3OO
i
~¢:'.
2OO 1(30 0
i
I
I
I
I
5
I0
5
I0
5
I
DAYS
FIG. 2. Mean number of bar presses for the three animals during each of the four phases, water, quinine, water, saccharin, as indicated by the vertical lines are presented before and after septal lesions. In an attempt to assess the effects of a comparable amount of tissue destruction in some other part of the brain a fourth animal was subjected to the ,same procedures. There were no observable effects of this lesion under these experimental conditions. The mean fluid intakes for water, quinine, and saccharin for the 10 day periods preoperatively were 25.2, 14.6, and 34.8 ml respectively and 25.7, 13.8, and 34.3 ml postoperatively. The corresponding mean number of bar presses were 367, 395, 342 and 370, 391, and 340. Histological examination revealed the control lesion to be restricted primarily to the lateral region of the posterior dorsal hypothalamus including the zona incerta and the ventral nucleus of the thalamus. In the other three animals extensive damage was produced primarily in the septa! nuclei with some destruction anterior and ventral into the diagonal bands of Broca with some sparing of the ventral portion of the posterior end of the lateral septat nuclei. DISCUSSION
Although the results of this experiment do not offer conclusive evidence they do indicate that the septum
SEPTAL LESIONS AND POLYDIPSIA
665
normally reduces the amount of schedule-induced polydipsia which develops in its absence and that it enhances the palatability modulation of schedule-induced drinking. Bar pressing was also enhanced by the septal lesions even when the animals were forced to drink the quinine solution. When the animals drink less because the fluid is made mildly aversive, they seem to become more excitable and press more. The effects with saccharin are also interesting because the animals drink more and press
less. The data on the fourth animal indicate that the effects are to be certain extent specific to the septum. These results therefore tend to support the hypothesis that these interesting schedule-induced effects on behavior are mediated via a septal interaction with the lateral hypothalamus. Additional support comes from the fact that the taste of the fluids also determines the degree of polydipsia which develops.
REFERENCES 1. 2. 3. 4.
Beatty, W. W. and J. S. Schwartzbaum. Enhanced reactivity to quinine and saccharin solutions following septal lesions in the rat. Psychon. Sci. 8: 483-484, 1967. Blass, E. M. and D. G. Hanson. Primary hyperdipsia in the rat following septal lesions. J. comp. physiol. Psychol. 70: 87-93, 1970. Carey, R. J. Quinine and saccharin preference-aversion threshold determinations in rats with septal ablations. J. comp. physiol. Psychol. 76: 316-326, 1971. Donovick, P. J., R. G. Burright and E. Zuromski. Localization of quinine aversion within the septum, habenula and interpeduncular nucleus of the rat. J. comp. physiol. Psychol. 71: 376-383, 1970.
5. 6. 7.
Falk, J. L. The nature and determinants of adjunctive behavior. PhysiolBehav. 6: 577-588. 1971. Miller,J. J. and G. J. Mogenson. Projections of the septum to the lateral hypothalamus. ExplNeurol. 34: 229-243, 1972. Wayner, M. J. Motor control functions of the lateral hypothalamus and adjunctive behavior. Physiol. Behav. 5: 1319-1325, 1970.
BRIEF COMMUNICATION Effects of Septal Lesions on Palatability Modulation of Schedule-Induced Polydipsia 12 M. J. WAYNER AND I. GREENBERG
Brain Research Laboratory, Syracuse University, 601 University Ave., Syracuse, N. Y. 13210 (Received 3 August 1972) WAYNER M. J. AND I. GREENBERG. Effects of septal lesions on palatability modulation of schedule.induced polydipsla. PHYSIOL. BEHAV. 9(4) 663-665, 1972.-The effects of rehtively large septal lesions on schedule-induced drinking of water, quinine hydroehloride, and saccharin solutions in three rats were determined. Results indicate that septal lesions enhance schedule-induced polydipsia and decrease an apparent palatability related inlu'bitory effect on drinking. The absence of these effects in one control animal with extensive damage in the dorsolateral portion of hypothalamus including the zona incerta and ventral thalamic nucleus suggests that these effects might be specific to the septum. Septum
Palatability
Schedule-induced polydipsia
Drinking
Procedure
SCHEDULE-INDUCED polydipsia has become a well documented phenomenon [5] which appears to be only one of a general class of behaviors which are adjunctive both with respect to physiological imbalance and reinforcement [7]. The fact that these behaviors might depend upon motor control functions of the lateral hypothalamus results in some interesting testable hypotheses. As the septum has been implicated in palatability mediated effects on fluid consumption [1, 3, 4], in the determination of water intake [2], and in the facilitation and inhibition of lateral hypothalamic electrical activity [6], it seems reasonable to assume that septal lesions might have some effect on schedule-induced polydipsia. The purpose of the present experiment was to determine the effects of relatively large septal lesions on schedule-induced drinking of water, quinine hydrochloride and saccharin solutions. Results indicate that s e p t a l l e s i o n s enhance schedule-induced polydipsia and decrease an apparent palatability related inhibitory effect on drinking.
Animals were reduced to 80% of their initial body weight and trained to respond on a FI-I min schedule for food reinforcement according to standard procedures in an LVE test chamber for one hr each day. Reinforcement consisted of 45 mg Noyes food pellets and water which was available in a stainless steel ball tipped drinking spout in the wall adjacent to the food delivery mechanism. Bar presses were recorded by conventional electromechanical equipment. Number of bar presses and water consumed during the test session and water intakes in the home cages and daily weights were measured. Water was present at all times in the home cage. After a bar press rate and schedule-induced polydipsia stabilized over a 10 day period, the water available during the test session was replaced with either a 0.008%, w/v, solution of quinine hydrochloride or a 0.05% o-benzoic sulfimide (saccharin) solution for the next 10 days. The order of presentation of the two solutions was varied for each rat. After 10 days of one or the other solution, it was replaced for two days with water, and then the water was replaced for the next 10 days with the other solution. At the end of this 32 day period, large bilateral septal lesions were produced in three animals by means of a temperature controlled radio frequency device. An attempt was made to
METHOD
Animals Four male Wistar rats, 3 0 0 - 4 0 0 g in weight, were selected and kept in individual living cages.
t This research was supported by NSF Grant GB-18414X and NIMH Grant 15473 and Training Grant MH-06969. 2We wish to acknowledge the help of E. Goodall who made the lesions in Dr. R. J. Carey's laboratory at the Syracuse Veterans Administration Hospital. 663
664
WAYNER AND GRk'.ENBtSR(;
destroy a comparable amount of tissue in tile posterior dorsomedial hypothalamus of a fourth animal which was to serve as a lesion control. On the day following surgery, animals were subjected to the same series of treatments in the same order. At the conclusion of the experiment animals were sacrificed with ether and perfused with 0.9% saline followed by 10% formalin. Brains were excised, frozen, cut serially at 60 u, stained with cresyl violet, and the e x t e n t of damage estimated by microscopic examination.
70-
HOH
QUININE
tHCYelt
SACCHARIN
5040.. . . ~ 0,4) • O~O, Je • O-O •
30-
g-4 O"~,OPRE OP O--OI~DST OP
20100
RESULTS
Results are summarized in Figs. 1 and 2. As all the animals with septal lesions displayed essentially the same effects, only the means for the three animals are presented. The mean fluid intakes for the animals during the test sessions are presented as a function of days in Fig. 1. Each 10 day period is presented serially from left to right. After the second 10 day period, water was returned for two days before the solution was changed for the next 10 days. The preoperative or base line data are indicated by solid circles and are connected by a solid line and the four phases of the experiment are indicated by the vertical bars. The postoperative means for similar treatments are indicated by solid circles connected by a broken line. The mean number of bar presses for the three animals are presented in a similar way in Fig. 2. The schedule-induced polydipsia during the first 10 days of the experiment remained relatively constant. Number of bar presses was also relatively stable during this period. When the water (HOH) was replaced with the quinine solution, schedule-induced polydipsia decreased and bar presses increased. When water was returned for two days, the polydipsia increased to the previous level and bar presses decreased. Saccharin produced an immediate and gradual increase in fluid consumption and a precipitous decrease in the number of bar presses. The same general effects were observed following the production of septal lesions except that the magnitude of the differences produced by the quinine and saccharin on fluid intake were attenuated and enhanced by saccharin on the number of bar presses for the last three days. Because of the small number of animals and the sequential nature of the data, only t-tests for correlated samples were calculated for each rat in an attempt to provide some measure of the reliability of the observations. The septal lesions produced a significant increase in the schedule-induced drinking of water in all three animals. The increase postoperatively cannot be attributed to the apparent carry-over of the increase which occurred with saccharin because the order of presentation was different for some animals. Quinine consumption decreased less following the lesions but decreased significantly for the three rats. The consumption of saccharin increased significantly following the lesions. Animals with septal lesions also pressed the bar more when water was available; the t-tests for all animals were significant. When quinine was presented the differences in number of bar presses was also significant. The two pronounced decreases in bar presses which occurred during the presentation of saccharin following the lesions are very obvious and were not associated with a decrease in fluid intake. The decrease was due primarily to decreases in consumption by two of the three animals.
i
60-
I
r
I
I
r
F
5
I0
5
10
5
10
DAYS
FIG. 1. Mean fluid intakes for the three animals during each of the four phases, water, quinine, water, saccharin, as indicated by the vertical lines are presented before and after septal lesions. 9O0
HOH
I
QUININ|
IHOI4[
SACCHARIN
II00 O-
- 0 I~ST OP
700
r,
P, A
o, 2, l~'*'°'°°'g'
6OO
i 1
3OO
i
~¢:'.
2OO 1(30 0
i
I
I
I
I
5
I0
5
I0
5
I
DAYS
FIG. 2. Mean number of bar presses for the three animals during each of the four phases, water, quinine, water, saccharin, as indicated by the vertical lines are presented before and after septal lesions. In an attempt to assess the effects of a comparable amount of tissue destruction in some other part of the brain a fourth animal was subjected to the ,same procedures. There were no observable effects of this lesion under these experimental conditions. The mean fluid intakes for water, quinine, and saccharin for the 10 day periods preoperatively were 25.2, 14.6, and 34.8 ml respectively and 25.7, 13.8, and 34.3 ml postoperatively. The corresponding mean number of bar presses were 367, 395, 342 and 370, 391, and 340. Histological examination revealed the control lesion to be restricted primarily to the lateral region of the posterior dorsal hypothalamus including the zona incerta and the ventral nucleus of the thalamus. In the other three animals extensive damage was produced primarily in the septa! nuclei with some destruction anterior and ventral into the diagonal bands of Broca with some sparing of the ventral portion of the posterior end of the lateral septat nuclei. DISCUSSION
Although the results of this experiment do not offer conclusive evidence they do indicate that the septum
SEPTAL LESIONS AND POLYDIPSIA
665
normally reduces the amount of schedule-induced polydipsia which develops in its absence and that it enhances the palatability modulation of schedule-induced drinking. Bar pressing was also enhanced by the septal lesions even when the animals were forced to drink the quinine solution. When the animals drink less because the fluid is made mildly aversive, they seem to become more excitable and press more. The effects with saccharin are also interesting because the animals drink more and press
less. The data on the fourth animal indicate that the effects are to be certain extent specific to the septum. These results therefore tend to support the hypothesis that these interesting schedule-induced effects on behavior are mediated via a septal interaction with the lateral hypothalamus. Additional support comes from the fact that the taste of the fluids also determines the degree of polydipsia which develops.
REFERENCES 1. 2. 3. 4.
Beatty, W. W. and J. S. Schwartzbaum. Enhanced reactivity to quinine and saccharin solutions following septal lesions in the rat. Psychon. Sci. 8: 483-484, 1967. Blass, E. M. and D. G. Hanson. Primary hyperdipsia in the rat following septal lesions. J. comp. physiol. Psychol. 70: 87-93, 1970. Carey, R. J. Quinine and saccharin preference-aversion threshold determinations in rats with septal ablations. J. comp. physiol. Psychol. 76: 316-326, 1971. Donovick, P. J., R. G. Burright and E. Zuromski. Localization of quinine aversion within the septum, habenula and interpeduncular nucleus of the rat. J. comp. physiol. Psychol. 71: 376-383, 1970.
5. 6. 7.
Falk, J. L. The nature and determinants of adjunctive behavior. PhysiolBehav. 6: 577-588. 1971. Miller,J. J. and G. J. Mogenson. Projections of the septum to the lateral hypothalamus. ExplNeurol. 34: 229-243, 1972. Wayner, M. J. Motor control functions of the lateral hypothalamus and adjunctive behavior. Physiol. Behav. 5: 1319-1325, 1970.