BEHAVIORALBIOLOGY, 13, 483-489 (1975), Abstract No. 4207
Fornicotomy: Effect on the Primary and Secondary Punishment of Mouse Killing by LiC1 Poisoning I JOHN M. DE CASTRO 2 and SAUL BALAGURA3
Department of Psychology, University of Massachusetts, Amherst, Massachusetts 01002
When paired with mouse killing LiC1 poisoning successfully inhibited mouse killing in the absence of prey ingestion. It was also demonstrated that subsequently the injection procedure could become a conditioned punisher, inhibiting mouse killing. Fomix lesions did not disrupt the primary inhibition of mouse killing but eliminated the secondary punishment effect. Implications for the neural circuitry of interspecific aggression are discussed.
Flynn and his co-workers (see Flynn, 1967, for review) have proposed that the hippocampus plays a "modulatory" role in the neurophysiological mechanism of interspecific aggression. They found that electrical stimulation of the hippocampus did not directly elicit attack behavior, rather it resulted in a modification of response latencies when attack was elicited by stimulation of the lateral hypothalamus. What is this "modulatory" role played by the hippocampus and what is its functional significance? Perhaps the hippocampus operates to modulate attack behavior according to prior operant learning. For example it could play a response inhibitory role (McCleary, 1966) by suppressing aggressive responses which in the past have been punished. It is also possible that the hippocampus operates to modulate attack behavior according to prior classical conditioning (Kimble, 1968; Mico and Schwartz, 1972). For example it could inhibit attack behavior in the presence of cues which in the past have been associated with punishment. The former hypothesis would predict that hippocampal destruction should impair the ability of an animal to inhibit attack behavior even when it 1This research was supported in part by NIMH Training Grant in Experimental Psychology (MH11823) to J. deC. and by a faculty research grant to S. B. 2Requests for reprints should be sent to John M. de Castro, Department of Psychology, Georgia State University, University Plaza, Atlanta, GA 30303. 3Now at Downstate Medical Center, Brooklyn, NY. 483 Copyright © 1975 by Academic Press, Inc. All rights of reproduction in any form reserved.
484
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had been previously punished. On the other hand the latter hypothesis would predict no impairment in the primary punishment effect but a deficit in the ability of secondary punishers to inhibit attack behavior. Mouse killing by rats can be inhibited or eliminated by making the rat ill (with a toxic but not lethal dose of a noxious agent such as Lithium Chloride, LiC1) following a kill (O'Boyle, 1973; Clody and Vogel, 1973). If the hippocampus plays a response inhibitory role in interspecific aggressive behavior, then its destruction should result in an impairment of the acquisition of a conditioned aversion to mouse killing. If, on the other hand, the hippocampus operates according to prior stimulus-stimulus (classical) conditioning, then its destruction should disrupt the inhibition of muricide 4 produced by cues associated with illness (e.g., the injection procedure). Since the hippocampus projects to the lateral hypothalamus by way of the fornix, it would appear likely that modulatory influences are transmitted via the fornix. Fornicotomy, then, should induce the same alterations of aggressive behavior as hippocampal destruction, without the added complication of disrupting the hippocampal-enthorinal connections. Hence, the following experiment was performed to test the above predictions by comparing the response of fornix lesioned and sham operated rats to the primary and second punishment of mouse killing. METHOD
Subjects. Twenty adult male Holtzman albino rats served as subjects. At the time of surgery they were 80-85 days old and weighed between 250 and 350 g. Surgery and Histology. Surgery was performed under sodium pentobarbital anesthesia (40 mg/kg) with atropine methyl nitrate (0.75 mg) given as premedication. Lesions were produced in ten animals while ten were given sham operations. The electrodes used were No. 00 stainless steel insect pins insulated with teflon except for 0.5 mm at the tip. Tubular damage, across the fimbria-fornix complex was achieved by producing five adjacent radio frequency lesions (Grass LM-4 radio frequency lesion maker, 100roW for 50 sec) through a coronal plane 1.4 mm posterior to bregma (skuU level between lambda and bregma), at a depth of 4.8 mm from the t o p of the skull, at lateral levels +1.7, +0.7, 0.0, -0.7, -1.7 mm with respect to the midsaggital sinus. The animals were sacrificed at the completion of testing and perfused through the heart with isotonic saline followed by 10% neutral buffered 4The word murieide is derived from muridae, a large class of rodents of the genus Mus including rats and mice. Its common, albeit inaccurate, usage in the psychological literature refers mostly to mouse killing.
FORNICOTOMY AND MOUSE KILLING INHIBITION
485
formalin. The brains were imbedded in gelatin and coronal sections were cut at 50 gm and stained with a modified Weigert method for unmounted sections (Wolf, 1971). Procedure. Five days postoperatively the rats were placed on a 1 hr per day feeding schedule for three days (water always available). On the third day a mouse was placed in the cage instead of the food and the time from presentation of the mouse to its death (kill latency) was recorded. Ad libitum food was again reinstated. One week later the animals were again deprived of food for 23 hr and the second mouse killing test was administered. Following one more week the third mouse killing test was given, this time under ad lib. feeding conditions. This procedure insured that all the rats became mouse killers. From then on mouse killing tests were given every four days to rats with ad lib. food. The mice were always removed immediately following the kill, preventing the rats from ingesting the mice. Animals were assigned to one of four groups: fornix lesioned-lithium chloride poisoned (Fornix-poison), fornix lesioned-saline control (Fornixcontrol), sham operated-lithium chloride poisoned (Sham-poison), and sham operated-saline control (Sham-control). Immediately following the fourth mouse killing test, rats were injected intraperitoneally (ip) with either 5 ml of 0.24MLiC1 or isotonic saline. Throughout the remainder of the experiment mouse killing tests were spaced apart by four days to insure the abatement of any residual drug effects. Fornix-poison and sham-poison animals were given LiC1 after every mouse kill until they refrained from killing with a 1 hr test period. The control rats received NaC1 injections following each kill as part of a yoked type paradigm. After successful inhibition of killing in the poisoned animals was attained, testing for conditioning to the injection procedure began. Muricide testing not followed by ip injections was continued every four days until mouse killing behavior reappeared in two consecutive tests. Immediately after the second kill, all four groups were given ip 5 ml injections of saline. Four days later, mouse killing was again tested. No injection was given after this test for conditioned effects. This cycle of muricide-saline injection, muricide-no saline injection was repeated three times.
RESULTS
Histology. The maximum and minimum extent of the brain damage for the lesioned animals is depicted in Fig. 1. The orientation of the lesion with respect to a three dimensional brain is also shown. Lesions involving the fornix just anterior to the hippocampus and posterior to the septum were observed in all ten animals. The anterior thalamic nuclei were damaged in three rats. The stria medullaris and corpus callosum were involved in another
486
DE CASTRO AND BALAGURA
Fig. 1. Maximum and minimum extent of the brain damage (left) and a threedimensional representation of the locus of the damage (right). three rats. Thus, the only structures incurring consistent damage were the fornical-septo-fimbrial area and the timbria fornix complex. Behavioral. The initial experimental paradigm, outlined in the methods section, resulted in consistent mouse killing behavior. Every animal, prior to punishment, killed every mouse presented. The LiC1 injections successfully inhibited mouse killing. All 10 LiC1 treated animals reached the learning criterion and refrained from killing during at least one test period. None of the non-poisoned control animals refrained from killing, most killed within 30 sec (the longest latency recorded was less than 4 rain). The primary inhibition of mouse killing induced by LiC1 poisoning was not disrupted by fornix lesions. All lesioned and all sham operated poisoned animals stopped killing and they did not differ in the number of injections required to produce criterion performance (Mean injections = 2.4 and 2.2 for sham-poison and fornix-poison groups respectively). After cessation of LiC1 injections following the attainment of the criterion, four out of the five animals in both groups returned to killing. One lesioned and one sham operated animal never again killed a mouse in 15 consecutive tests. Once again the lesioned and control animals did not differ in the number of nonpoisoned sessions required to reinstate mouse killing (Mean sessions = 1.3 and 1.5 for sham-poison and fornix-poison groups respectively). Secondary punishment effects on the reinstated mouse killing response attributable to the injection procedure were analysed by comparing the latency to kill prior to the saline injection with the latency to kill four days later. Graphical representation of the median change in latency for all groups is depicted in Fig. 2. Kruskal-Wallis one-way analysis of variance for ranked data revealed significant group effects on the first two secondary punishment tests (H (3) = 7.85, P < 0~05; H (3) = 8.38, P < 0.05 respectively). Analysis of individual groups effects with Dunn's post hoc test revealed that the sham-
FORNICOTOMY AND MOUSE KILLING INHIBITION
25
487
• • SHAM - POISON • .......... • FORNIX- POISON r'l I"1 SHAM - CONTROL I"1.......... rl FORNIX-CONTROL
20
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°o°°,°°°°°°°°'°°'°°
I 1
I 2 SECONDARY
PUNISHMENT
I 3 TEST
Fig. 2. The median latency change for each group over the three secondary punishment tests.
poison group differed significantly from all other groups (Y/O = 12.85, P < 0 . 0 5 ; Y/O = 11.04, P < 0 . 0 5 , for tests 1 and 2 respectively). The sham-poison group significantly differed from the sham control group (Y/O = 2.67, P < 0.05 ; Y/O = 2.82, P < 0.05, for tests 1 and 2 respectively) while the fornix-poison group did not differ from the fornix control group (Y/O = 0.0; .-0.15; for test 1 and 2 respectively). There were no significant differences between the two control groups. A significant inverse relationship was found between the extent of the damage to the fornix and the change in latency to kill a mouse on the first secondary punishment test (Rank Order Correlation Coefficient = - 1 . 0 , P < 0 . 0 5 ) . Hence damage to the fornix, disrupted the effectiveness of a secondary punisher to affect kilt latencies, and the degree of disruption was related to the extent of the damage to the fornix.
488
DE CASTRO AND BALAGURA DISCUSSION
The present experiment demonstrated that LiC1 poisoning is effective in inhibiting the mouse killing response in the absence of prey ingestion. This phenomenon demonstrated in mammals in the present experiment and in previous investigations (O'Boyle, 1973; Clody and Vogel, 1973), appears to be similar to the aversions to poisonous monarch butterflies obtained in bluejays under natural conditions (Brower and Brower, 1964). Lesions of the fornix did not affect the primary inhibition of mouse killing by lithium chloride. Although there is evidence that the hippocampus does play a role in taste aversions, the published evidence concerning the locus within the laippocampus responsible for this function is at best equivocal (Miller, Elkins and Peacock, 1971; McGowan, Hankins and Garcia, 1972; Best and Orr, 1973) and have used vastly different methods and tasks. We can conclude though, that under the present experimental conditions, the hippocampal system mediated by the fornix is not necessary for the acquisition of a primary learned aversion or for its subsequent extinction. Furthermore, since fornix lesioned animals were just as capable as non-lesioned animals at learning to withhold the punished interspecific aggressive response, we can also conclude that the hippocampal-fornix system does not modulate interspecific aggression by suppressing responses which previously have been punished (response inhibition). Sham-poison animals demonstrated a significant conditioned response to the injection procedure (secondary punishment effect). They increased their latency to kill a mouse even four days after a saline injection had followed the previous kill. These results are compatible with those of other investigators (Best, Best and Mickley, 1973) who demonstrated a similar secondary punishment effect to environmental stimuli (black compartment). In contrast to the sham operated animals, the fornix lesioned animals failed to show a conditioned response to the injection procedure. There were no signifcant changes in their kill latencies following the saline injections. In addition this deficit was found to be correlated with the extent of the damage to the fornix. Hence, fornix lesions prevented a stimulus, previously associated with punishment, from exerting an inhibitory influence on the mouse killing response. This finding supports the hypothesis that the hippocampal-fornix system acts to modulate interspecific aggressive behavior in the presence of stimuli which in the past have been associated with an aversive event. REFERENCES Best, P. J., Best, M. R., and Mickley, G. A. (1973). Conditioned aversion to distinct environmental stimuli resulting from gastrointestinal distress. 2". Comp. Physiol. Psyehol. 85, 250-257.
FORNICOTOMY AND MOUSE KILLING INHIBITION
489
Best, P. J., and Orr, J. (1973). Effects of hippocampal lesions on passive avoidance and taste aversion conditioning. PhysioL Behav. 10, 193-196. Brower, L. P., and Brower, J. V. Z. (1964). Birds, butterflies, and plant poisons: a study of ecological chemistry. Zoologica: New York Zoological Society 49, 137-159. Clody, D. E., and Vogel, J. R. (1973). Drug induced conditioned aversion to mouse killing in rats. Pharm. Biochem. Behav. 1,477-481. Flynn, J. P. (1967). The neural basis of aggression in cats. In D. C. Glass (Ed.), "Neurophysiology and Emotion," pp. 40-60. New York: Rockefeller University Press. Kimble, D. P. (1968). The hippocampus and internal inhibition. Psych. Bull. 70, 285-295. McCleary, R. A. (1966). Response modulatory functions of the limbic system: initiation and suppression. In E. Stellar and J. M. Sprague (Eds.), "Progress in Physiological Psychology," pp. 290-292. New York: Academic Press. McGowan, B. K., Hankins, W. G., and Garcia, J. (1972). Limbic lesions and the control of the internal and external environment. Behav. BioL 7, 841-852. Mico, D. J., and Schwartz, M. (1972). Effects of hippocampal lesions on the development of pavlovian internal inhibition in rats. J. Comp. Physiol. Psychol. 76, 371-377. Miller, C. R., Elkins, R. L., and Peacock, L. J. (1971). Disruption of a radiation-induced preference shift by hippocampal lesions. Physiol. Behav. 6,283-285. O'Boyle, M. (1973). Suppression and recovery of mouse killing in rats following punishment with lithium chloride injections. Paper presented at the Eastern Psychological Association Meeting, Washington, D.C., May, 1973. Wolf, G. (1971). Elementary histology for neuropsychologists. In R. D. Myers (Ed.), "Methods in Psychobiology," pp. 281-300. New York: Academic Press.
Fornicotomy: Effect on the Primary and Secondary Punishment of Mouse Killing by LiC1 Poisoning I JOHN M. DE CASTRO 2 and SAUL BALAGURA3
Department of Psychology, University of Massachusetts, Amherst, Massachusetts 01002
When paired with mouse killing LiC1 poisoning successfully inhibited mouse killing in the absence of prey ingestion. It was also demonstrated that subsequently the injection procedure could become a conditioned punisher, inhibiting mouse killing. Fomix lesions did not disrupt the primary inhibition of mouse killing but eliminated the secondary punishment effect. Implications for the neural circuitry of interspecific aggression are discussed.
Flynn and his co-workers (see Flynn, 1967, for review) have proposed that the hippocampus plays a "modulatory" role in the neurophysiological mechanism of interspecific aggression. They found that electrical stimulation of the hippocampus did not directly elicit attack behavior, rather it resulted in a modification of response latencies when attack was elicited by stimulation of the lateral hypothalamus. What is this "modulatory" role played by the hippocampus and what is its functional significance? Perhaps the hippocampus operates to modulate attack behavior according to prior operant learning. For example it could play a response inhibitory role (McCleary, 1966) by suppressing aggressive responses which in the past have been punished. It is also possible that the hippocampus operates to modulate attack behavior according to prior classical conditioning (Kimble, 1968; Mico and Schwartz, 1972). For example it could inhibit attack behavior in the presence of cues which in the past have been associated with punishment. The former hypothesis would predict that hippocampal destruction should impair the ability of an animal to inhibit attack behavior even when it 1This research was supported in part by NIMH Training Grant in Experimental Psychology (MH11823) to J. deC. and by a faculty research grant to S. B. 2Requests for reprints should be sent to John M. de Castro, Department of Psychology, Georgia State University, University Plaza, Atlanta, GA 30303. 3Now at Downstate Medical Center, Brooklyn, NY. 483 Copyright © 1975 by Academic Press, Inc. All rights of reproduction in any form reserved.
484
DE CASTRO AND BALAGURA
had been previously punished. On the other hand the latter hypothesis would predict no impairment in the primary punishment effect but a deficit in the ability of secondary punishers to inhibit attack behavior. Mouse killing by rats can be inhibited or eliminated by making the rat ill (with a toxic but not lethal dose of a noxious agent such as Lithium Chloride, LiC1) following a kill (O'Boyle, 1973; Clody and Vogel, 1973). If the hippocampus plays a response inhibitory role in interspecific aggressive behavior, then its destruction should result in an impairment of the acquisition of a conditioned aversion to mouse killing. If, on the other hand, the hippocampus operates according to prior stimulus-stimulus (classical) conditioning, then its destruction should disrupt the inhibition of muricide 4 produced by cues associated with illness (e.g., the injection procedure). Since the hippocampus projects to the lateral hypothalamus by way of the fornix, it would appear likely that modulatory influences are transmitted via the fornix. Fornicotomy, then, should induce the same alterations of aggressive behavior as hippocampal destruction, without the added complication of disrupting the hippocampal-enthorinal connections. Hence, the following experiment was performed to test the above predictions by comparing the response of fornix lesioned and sham operated rats to the primary and second punishment of mouse killing. METHOD
Subjects. Twenty adult male Holtzman albino rats served as subjects. At the time of surgery they were 80-85 days old and weighed between 250 and 350 g. Surgery and Histology. Surgery was performed under sodium pentobarbital anesthesia (40 mg/kg) with atropine methyl nitrate (0.75 mg) given as premedication. Lesions were produced in ten animals while ten were given sham operations. The electrodes used were No. 00 stainless steel insect pins insulated with teflon except for 0.5 mm at the tip. Tubular damage, across the fimbria-fornix complex was achieved by producing five adjacent radio frequency lesions (Grass LM-4 radio frequency lesion maker, 100roW for 50 sec) through a coronal plane 1.4 mm posterior to bregma (skuU level between lambda and bregma), at a depth of 4.8 mm from the t o p of the skull, at lateral levels +1.7, +0.7, 0.0, -0.7, -1.7 mm with respect to the midsaggital sinus. The animals were sacrificed at the completion of testing and perfused through the heart with isotonic saline followed by 10% neutral buffered 4The word murieide is derived from muridae, a large class of rodents of the genus Mus including rats and mice. Its common, albeit inaccurate, usage in the psychological literature refers mostly to mouse killing.
FORNICOTOMY AND MOUSE KILLING INHIBITION
485
formalin. The brains were imbedded in gelatin and coronal sections were cut at 50 gm and stained with a modified Weigert method for unmounted sections (Wolf, 1971). Procedure. Five days postoperatively the rats were placed on a 1 hr per day feeding schedule for three days (water always available). On the third day a mouse was placed in the cage instead of the food and the time from presentation of the mouse to its death (kill latency) was recorded. Ad libitum food was again reinstated. One week later the animals were again deprived of food for 23 hr and the second mouse killing test was administered. Following one more week the third mouse killing test was given, this time under ad lib. feeding conditions. This procedure insured that all the rats became mouse killers. From then on mouse killing tests were given every four days to rats with ad lib. food. The mice were always removed immediately following the kill, preventing the rats from ingesting the mice. Animals were assigned to one of four groups: fornix lesioned-lithium chloride poisoned (Fornix-poison), fornix lesioned-saline control (Fornixcontrol), sham operated-lithium chloride poisoned (Sham-poison), and sham operated-saline control (Sham-control). Immediately following the fourth mouse killing test, rats were injected intraperitoneally (ip) with either 5 ml of 0.24MLiC1 or isotonic saline. Throughout the remainder of the experiment mouse killing tests were spaced apart by four days to insure the abatement of any residual drug effects. Fornix-poison and sham-poison animals were given LiC1 after every mouse kill until they refrained from killing with a 1 hr test period. The control rats received NaC1 injections following each kill as part of a yoked type paradigm. After successful inhibition of killing in the poisoned animals was attained, testing for conditioning to the injection procedure began. Muricide testing not followed by ip injections was continued every four days until mouse killing behavior reappeared in two consecutive tests. Immediately after the second kill, all four groups were given ip 5 ml injections of saline. Four days later, mouse killing was again tested. No injection was given after this test for conditioned effects. This cycle of muricide-saline injection, muricide-no saline injection was repeated three times.
RESULTS
Histology. The maximum and minimum extent of the brain damage for the lesioned animals is depicted in Fig. 1. The orientation of the lesion with respect to a three dimensional brain is also shown. Lesions involving the fornix just anterior to the hippocampus and posterior to the septum were observed in all ten animals. The anterior thalamic nuclei were damaged in three rats. The stria medullaris and corpus callosum were involved in another
486
DE CASTRO AND BALAGURA
Fig. 1. Maximum and minimum extent of the brain damage (left) and a threedimensional representation of the locus of the damage (right). three rats. Thus, the only structures incurring consistent damage were the fornical-septo-fimbrial area and the timbria fornix complex. Behavioral. The initial experimental paradigm, outlined in the methods section, resulted in consistent mouse killing behavior. Every animal, prior to punishment, killed every mouse presented. The LiC1 injections successfully inhibited mouse killing. All 10 LiC1 treated animals reached the learning criterion and refrained from killing during at least one test period. None of the non-poisoned control animals refrained from killing, most killed within 30 sec (the longest latency recorded was less than 4 rain). The primary inhibition of mouse killing induced by LiC1 poisoning was not disrupted by fornix lesions. All lesioned and all sham operated poisoned animals stopped killing and they did not differ in the number of injections required to produce criterion performance (Mean injections = 2.4 and 2.2 for sham-poison and fornix-poison groups respectively). After cessation of LiC1 injections following the attainment of the criterion, four out of the five animals in both groups returned to killing. One lesioned and one sham operated animal never again killed a mouse in 15 consecutive tests. Once again the lesioned and control animals did not differ in the number of nonpoisoned sessions required to reinstate mouse killing (Mean sessions = 1.3 and 1.5 for sham-poison and fornix-poison groups respectively). Secondary punishment effects on the reinstated mouse killing response attributable to the injection procedure were analysed by comparing the latency to kill prior to the saline injection with the latency to kill four days later. Graphical representation of the median change in latency for all groups is depicted in Fig. 2. Kruskal-Wallis one-way analysis of variance for ranked data revealed significant group effects on the first two secondary punishment tests (H (3) = 7.85, P < 0~05; H (3) = 8.38, P < 0.05 respectively). Analysis of individual groups effects with Dunn's post hoc test revealed that the sham-
FORNICOTOMY AND MOUSE KILLING INHIBITION
25
487
• • SHAM - POISON • .......... • FORNIX- POISON r'l I"1 SHAM - CONTROL I"1.......... rl FORNIX-CONTROL
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°o°°,°°°°°°°°'°°'°°
I 1
I 2 SECONDARY
PUNISHMENT
I 3 TEST
Fig. 2. The median latency change for each group over the three secondary punishment tests.
poison group differed significantly from all other groups (Y/O = 12.85, P < 0 . 0 5 ; Y/O = 11.04, P < 0 . 0 5 , for tests 1 and 2 respectively). The sham-poison group significantly differed from the sham control group (Y/O = 2.67, P < 0.05 ; Y/O = 2.82, P < 0.05, for tests 1 and 2 respectively) while the fornix-poison group did not differ from the fornix control group (Y/O = 0.0; .-0.15; for test 1 and 2 respectively). There were no significant differences between the two control groups. A significant inverse relationship was found between the extent of the damage to the fornix and the change in latency to kill a mouse on the first secondary punishment test (Rank Order Correlation Coefficient = - 1 . 0 , P < 0 . 0 5 ) . Hence damage to the fornix, disrupted the effectiveness of a secondary punisher to affect kilt latencies, and the degree of disruption was related to the extent of the damage to the fornix.
488
DE CASTRO AND BALAGURA DISCUSSION
The present experiment demonstrated that LiC1 poisoning is effective in inhibiting the mouse killing response in the absence of prey ingestion. This phenomenon demonstrated in mammals in the present experiment and in previous investigations (O'Boyle, 1973; Clody and Vogel, 1973), appears to be similar to the aversions to poisonous monarch butterflies obtained in bluejays under natural conditions (Brower and Brower, 1964). Lesions of the fornix did not affect the primary inhibition of mouse killing by lithium chloride. Although there is evidence that the hippocampus does play a role in taste aversions, the published evidence concerning the locus within the laippocampus responsible for this function is at best equivocal (Miller, Elkins and Peacock, 1971; McGowan, Hankins and Garcia, 1972; Best and Orr, 1973) and have used vastly different methods and tasks. We can conclude though, that under the present experimental conditions, the hippocampal system mediated by the fornix is not necessary for the acquisition of a primary learned aversion or for its subsequent extinction. Furthermore, since fornix lesioned animals were just as capable as non-lesioned animals at learning to withhold the punished interspecific aggressive response, we can also conclude that the hippocampal-fornix system does not modulate interspecific aggression by suppressing responses which previously have been punished (response inhibition). Sham-poison animals demonstrated a significant conditioned response to the injection procedure (secondary punishment effect). They increased their latency to kill a mouse even four days after a saline injection had followed the previous kill. These results are compatible with those of other investigators (Best, Best and Mickley, 1973) who demonstrated a similar secondary punishment effect to environmental stimuli (black compartment). In contrast to the sham operated animals, the fornix lesioned animals failed to show a conditioned response to the injection procedure. There were no signifcant changes in their kill latencies following the saline injections. In addition this deficit was found to be correlated with the extent of the damage to the fornix. Hence, fornix lesions prevented a stimulus, previously associated with punishment, from exerting an inhibitory influence on the mouse killing response. This finding supports the hypothesis that the hippocampal-fornix system acts to modulate interspecific aggressive behavior in the presence of stimuli which in the past have been associated with an aversive event. REFERENCES Best, P. J., Best, M. R., and Mickley, G. A. (1973). Conditioned aversion to distinct environmental stimuli resulting from gastrointestinal distress. 2". Comp. Physiol. Psyehol. 85, 250-257.
FORNICOTOMY AND MOUSE KILLING INHIBITION
489
Best, P. J., and Orr, J. (1973). Effects of hippocampal lesions on passive avoidance and taste aversion conditioning. PhysioL Behav. 10, 193-196. Brower, L. P., and Brower, J. V. Z. (1964). Birds, butterflies, and plant poisons: a study of ecological chemistry. Zoologica: New York Zoological Society 49, 137-159. Clody, D. E., and Vogel, J. R. (1973). Drug induced conditioned aversion to mouse killing in rats. Pharm. Biochem. Behav. 1,477-481. Flynn, J. P. (1967). The neural basis of aggression in cats. In D. C. Glass (Ed.), "Neurophysiology and Emotion," pp. 40-60. New York: Rockefeller University Press. Kimble, D. P. (1968). The hippocampus and internal inhibition. Psych. Bull. 70, 285-295. McCleary, R. A. (1966). Response modulatory functions of the limbic system: initiation and suppression. In E. Stellar and J. M. Sprague (Eds.), "Progress in Physiological Psychology," pp. 290-292. New York: Academic Press. McGowan, B. K., Hankins, W. G., and Garcia, J. (1972). Limbic lesions and the control of the internal and external environment. Behav. BioL 7, 841-852. Mico, D. J., and Schwartz, M. (1972). Effects of hippocampal lesions on the development of pavlovian internal inhibition in rats. J. Comp. Physiol. Psychol. 76, 371-377. Miller, C. R., Elkins, R. L., and Peacock, L. J. (1971). Disruption of a radiation-induced preference shift by hippocampal lesions. Physiol. Behav. 6,283-285. O'Boyle, M. (1973). Suppression and recovery of mouse killing in rats following punishment with lithium chloride injections. Paper presented at the Eastern Psychological Association Meeting, Washington, D.C., May, 1973. Wolf, G. (1971). Elementary histology for neuropsychologists. In R. D. Myers (Ed.), "Methods in Psychobiology," pp. 281-300. New York: Academic Press.
