Septal ablation and the social behavior of the golden hamster

Physiology and Behavior. Vol. 5, pp. 79-88. Pergamon Press, 1970. Printed in Great Britain

Septal Ablation and the Social Behavior of the Golden Hamster F R A N K J. S O D E T Z ~

Center for Neurobiological ,Sciences, University of Florida, Gainesville, Florida AND B. N. B U N N E L L

Department of Psychology, University of Georgia, Athens, Georgia (Received 28 July 1969)

SODETZ,F. J. and B. N. BUNNELL. Septal ablation and the social behavior of the golden hamster. PItYSIOL.BEHAV. 5 (1) 79--88, 1970.--In four experiments, the effect of septal ablation on the social behavior of the hamster was observed. The results indicated that septal ablation increased the aggressiveness of both socially naive and experienced dominant hamsters. If, however, the septal hamster experienced defeat by an opponent during preoperative testing, no postoperative increment in aggression was observed. All septal hamsters, whether aggressive or not, either ceased to display hoarding behavior or hoarded very little. All septal hamsters also showed persistent approach responses to their opponents. Paired contests between septal animals resulted in high levels of aggression with one septal in each pair being defeated and assuming a submissive status. Septal lesions Hamster Social behavior

Social dominance

Aggression

Social experience

Hoarding

Limbic system

aggressive behavior which results in the establishment of dominant-subordinate social relationships. The hamster was selected as the subject of study largely because of its tendency to readily initiate social activity upon coming in contact with conspecifics, its use of a limited number of discrete behaviors in its social interaction, and the availability of a method for assessing the effects of brain lesions on its behavior [7].

IN THEIR definitive report on the effects of septal ablation in the rat, Brady and Nanta [3] noted an increase in both intraand interspecific aggression in their experimental animals. Ensuing studies have implicated the septal region in the mediation of several classes of aggressive behavior such as those described by Meyer [13]. Increased predatory aggression was reported by Karli [8] who observed that rats which rarely killed mice in preoperative testing did so readily following septal ablation. Changes in irritable aggression following surgery have been observed in septal rats using the shockelicited aggression procedure of Ulrich and Azrin [17]. These have included reduced latency and increased frequency and intensity of attacking and fighting [1, 2]. Increases in spontaneous intermale aggression have also been observed [5, 6], but in these studies, some subjects displayed increases in defensive and escape behavior as well. The latter observation suggests that the septal region may he involved in the control of a broader spectrum of social behavior. Thomas, Hostetter and Barker [16] have reviewed the role of the limbic system in species-specific behavior and have summarized evidence implicating the septal region in the control of both maternal and copulatory behavior. The present series of experiments was designed to examine the effects of septal ablation on a variety of social and nonsocial behaviors in subjects with differing preoperative and social histories. A major emphasis was placed upon determining the role of the septal region in the regulation of that

METHOD

A general statement of the methodology used in the four experiments of the present study is presented below. Specific methodological details are discussed in the introductory statement preceding each of the experiments.

Subjects The subjects in the present study were 106 male Syrian golden hamsters obtained as weanlings from Manor Farms, Staxttsburg, New York. Within 3 days of their arrival in the laboratory the animals were separated and housed individually in single cages. Each animal had food, water and paper nesting materials continuously available through the entire period spent in the laboratory. When the animals reached an age of from 90 to 120 days they were assigned to matched weight ( 4-10 g) pairs and transferred from their single cages to individual compartments in the test apparatus. At no time

1Supported by grants B-1149 and B-4604 from the National Science Foundation. The services of the computing centers at the University of Florida and the University of Georgia are gratefully acknowledged. 2Present address: Department of Experimental Psychology, Walter Reed Army Institute of Research, Washington, D.C. 20012. 79

SODETZ AND BUNNELL

80 was an animal permitted to interact with another animal, except during the observation periods programmed for a given experiment. All handling of the animals was held to a minimum.

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Apparatus Two types of apparatus, which allowed the animals to live in the same environment in which they were tested, were used in the study. Experiments 1 and 2 were run using the test cage schematized in Fig. 1A. It consisted of a wire-mesh box divided into 3 compartments by 2 metal partitions. One member of each pair of animals lived in each of the end compartments (C) while the center compartment served as a neutral area (N). During testing, guillotine doors (G) in the partitions were raised permitting free access to all compartments by both animals. In Experiments 3 and 4 the apparatus schematized in Fig. 1B was used. This apparatus consisted of 6 living-cages (C) surrounding a neutral center area (N). During testing, any 2 animals could be permitted to interact by raising 2 of the 6 guillotine doors (G).

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Behavior Inventory In the development and standardization of the behavioral inventory used in the present study, the initial trials were conducted between pairs of animals. At first, observation periods of from 5-30 min per pair were used. Later, 3-6 animals were released simultaneously and their behaviors noted continuously over periods of up to 48 hr. Written records, supplemented by motion pictures, were made of the behaviors observed. These consisted of a notation of both the behavior and location at which it took place (i.e. home cage, opponent's cage, or in the central "neutral area of the apparatus"). Analysis of these written descriptions yielded a set of descriptive behavioral categories which were then tried out on a new population of the subjects composed of animals with varying kinds of early social experience. These data were then used to effect a final revision of the behavioral inventory. The inventory, together with the code symbols of each behavior, is presented in Table 1. The behaviors can be categorized as

V °'\/,, TWO IN.

FIG. 1. Schematic diagram of the floor plan of the two types of test cage used in the present study. Home cages (C), center or"neutral area" (N), and guillotine doors (G) are identified, social and non-social. A further division into: functional categories has been made and each functional category contains one or more subcategories representing the postures, movements, gestures, etc. which can be observed in the interaction of 2 adult male hamsters.

Behavioral Testing Except where noted, members of a pair encountered only each other throughout the course of a given experiment.

TABLE 1 HAMSTER BEHAVIOR--FREEINTERACTIONSOCIALTEST (FIST) INVENTORY Nonsocial E --Locomotor exploratory G --Self grooming UA--Picking up, pouching, or carrying nest materials HA--Piling, arranging nest materials in home cage UO--Picking up, pouching, or carrying food HO---Piling, arranging food in Home cage Miscellaneous V --Vocalization HC--Enters home cage* OC--Enters opponent's cage* M --Enters center (neutral) area*

Aggressive A --Attack posture (upright) A'--Attack posture (underneath) B ---Bite C --Chase Submissive T --Tail lift T'--Tail lift with adduction of hindleg Z --Freeze (lying on back, immobile) W--Attempted escape from cage (climbing, clinging to wall or ceiling) L - - F l i g h t (rapid exit from cage when opponent is present)

*Used to indicate place where other events scored on the inventory take place.

Social Orienting/Investigatory --Attend (turn head, or head and body toward opponent) N --Sniff opponent's head or body (requires physical contact) N ' --Sniff opponent's anogenital region (contact required) l

Defence P --Defensive posture (upright) P' --Defensive posture (side) Fighting S --Spar F --Fight X/Y Pins opponent to floor with front legs Y/X--Is pinned by opponent

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SEPTAL ABLATION AND BEHAVIOR The general procedure consisted of running each pair of animals 1 session a day. A session consisted of 5 rain of unrestricted interaction between members of a pair. This was accomplished by raising the guillotine doors separating the animals from the central area. Two trained observers, one for each animal, recorded the behavior observed during each session by writing down the code symbol for each behavior as it occurred. At the same time, the observer depressed a key which actuated a pen, assigned to his animal, on a multichannel event recorder. One channel on the recorder served as a time base. By collating the written response record with the output of the recorder, each session could be reconstructed with all behaviors for both animals in the proper temporal relationship to one another. The reconstruction of the sessions and analysis of the data were accomplished by computer.

Surgery and Histology All surgery was performed under sodium pentobarbital anesthesia (90 mg/kg) with atropine sulphate used to reduce respiratory complications. Bilateral radio frequency (RF) lesions of the septal region were placed stereotaxically using coordinates determined empirically in a series of pilot animals. In each experiment 2 types of control operations were used. In several animals a small bilateral R F lesion was placed in the nee- and cingulate cortex at the same anterior-posterior coordinates used for the septal lesions. In most animals, the control procedure consisted of bilateral insertion of the electrode to a point immediately dorsal to the septal region. N o lesion other than the electrode track was intentionally produced in this procedure. At the conclusion of the study, all animals were sacrificed. Cell and fiber stains were used to determine the locus and extent of the lesions. A representative septal and a control lesion are presented in Fig. 2. Bilateral damage to both medial and lateral septal nuclei was present in all 29 animals given septal lesions. In most cases this damage exceeded 80 per cent of these structures. What tissue was spared was usually located bilaterally in t h e caudal one-fifth of lateral septal nuclei. In all cases both the pre- and post-commissural fornix were sectioned bilaterally. Some damage to the ventral surface of the corpus caUosum was present in all lesioned animals as was damage to the anterior commissure. In the majority of animals, there was subtotal bilateral destruction of the bed nucleus of the stria terminalis. In some animals the caudate nuclei, anterior limbic cortex, genu of the corpus caUosu, preoptic region, body of the fornix, or rostrodorsal thalamus sustained some damage. However, no consistent pattern of damage was noted for these non-septal structures. The control lesions were confined to the cingulate and neecortex at the level shown in Fig. 2. In some animals there was damage to both the corpus callosum and cingulum. EXPERIMENT 1

Eleven pairs of hamsters were used in Experiment 1. The experiment was designed to permit observation of the lesion effect without potential confounding by preoperative social experience. F r o m weaning all of the animals were raised in social isolation. Two weeks before the initiation of testing, 1 randomly selected member of each of 6 pairs underwent surgery and received a bilateral septal lesion. Their opponents underwent one of the control procedures described above.

81 Neither member of the remaining 5 pairs was operated. These animals served as a normal control group. Following a twoweek post-operative recovery period, testing was begun. It consisted of observing each pair for one daily 5-rain session on each of 5 consecutive days. None of the animals had had an opportunity to interact with one another at any time before the initiation of testing.

Results The results of Experiment 1 are summarized in Fig. 3. The individual behaviors included in the inventory have been combined with others in their respective functional subcategories. Each data point represents the proportion of the total number of responses observed during a given session which fell into a given functional subcategory. The 4 curves presented in each figure represent the septal group (n = 6), the opponents of the septal animals (n = 6), the normal dominant animals (n = 5), and their submissive opponents (n = 5), The data on the observed incidence of fighting are presented in Fig. 3A. The mean proportion of fighting averaged over all sessions was 0.19 in the pairs in which one member was a septal. The proportion of fighting in the normal control pairs was 0.05. The difference was evaluated with a test for the significance of a difference between proportions [12] (Z = 8.01. p < 0.001). The experimental group consistently showed a greater proportion of fighting behavior. Other aspects of the interactions are reflected in the remaining figures. Figure 3B presents the data on aggressive behavior excluding fighting. This category includes those behaviors employed in the initiation of fighting. F o r any given session, no less than 25 per cent of all of the behavior of the septal animals was aggressive. Their control opponents, however, never displayed more than 3 per cent aggression following the first session. This difference between the amount of aggression displayed by septals and their opponents was significant (Z = 35.00, p < 0.001). In each of the control pairs, 1 member consistently displayed more aggression than its opponent. Collectively these animals have been labelled the dominant normal group. The difference in the amount of agression displayed by them and their opponents was also statistically significant (Z = 21.93, p < 0.001). A comparison between the septal group which never displayed less than 25 per cent aggression and the dominant normal group which never displayed more than 15 per cent aggression indicated that although both groups were substantially more aggressive than their opponents, the septals were consistently more aggressive than the dominant normal animals. Figure 3C presents the data on submissive behavior. Both groups of dominant animals display few submissive responses. The proportion of submissive behavior observed in the group which opposed dominant normal animals was not large; however, the difference between them and their opponents was significant (Z = 12.00, p < 0.001). Similarly, the animals opposing septals displayed more submissive behavior than their lesioned opponents. A comparison between these two groups of submissive animals was also significant (Z = 20.87, p < 0.001). Those animals which opposed the highly aggressive septals displayed more submissive behavior. Figure 3D, which presents the data from observations of flight and escape behaviors is similar to that for submission (Fig. 3C). Both the septals and dominant normals showed little of this behavior and significantly loss than their respective opponents. As was the case for submission, the animals opposing the septals displayed significantly more escape

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behavior than did those with normal opponents (Z = 16.24, p < 0,001). Defensive behavior was displayed by all groups in the experiment (Fig. 3E). However, significantly more defensive behavior was observed in the submissive groups (Z = 19.82, p < 0,001). The social investigatory (Fig. 2F) includes behaviors which require an animal to initiate physical contact with an opponent. Submissive animals, therefore, are less likely to engage in this kind of activity. A comparison of all submissive animals with all dominant animals (Z = 67.12, p < 0.001) confirmed this observation. Septal animals, however, engaged in more of this behavior than did the dominant normal animals (Z = 2.61, p < 0.001). Figure 3G presents the data on general exploratory activity. The pairs in which 1 member was a septal displayed proportionately less of this behavior than did the normal pairs (Z = 23.88, p < 0.001). Hoarding, the other non-social category, is presented in Fig. 3H. Only a few hoarding responses were observed in the septal group, while all 3 remaining groups engaged in this behavior. A sharp increase over sessions was observed in the normal pairs. By the fifth session, nearly onethird of all the behaviors observed in this category. In the septal group, however, hoarding never exceeded 1 per cent of total behavior observed.

Conclusions Septal ablation in the socially naive animal appears to result in an inordinate display of aggression, both real and threatened, culminating in the defeat of opponents. In addition to the observed increase in aggressiveness, a significant change

in social investigatory behavior (exploratory sniffmg and pawing of an opponent) was also observed. Differences wore also found in the behavior of the opponents of the septal animals. The most pronounced difference was increased fiequency of escape behavior which may have reflected either the increased aggression of the septal animals or their persistent approach behavior noted in the social investigatory category. The lesion also modified the non-social behavior of the septal group. This took the form of a reduction in hoarding behavior. The level of hoarding behavior of their submissive opponents was also unusually low; however, this may have been the result of the intensity of the aggression they encountered. Hoarding requires that the animal leave its home cage and enter its opponent's cage to gather food and nesting materials. The submissive animals may have been restrained from doing so by the possibility of coming into physical contact with their dominant septal opponents. EXPERIMENT 2

The results of Experiment 1 suggested that the effect o f septal ablation in the hamster was increased aggressive and social investigatory behavior and a reduction in hoarding behavior. Experiment 2 was designed to evaluate the effects of septal ablation in animals with preoperative social experience. Because the observed effect in experiment one had been increased aggression, it was decided that the lesion should be administered to preoperatively submissive animals. The 5 normal pairs of hamsters which served as a control group in Experiment 1 were used:as the lesion group in Experiment 2.

SEPTAL ABLATION AND BEHAVIOR

83

These animals had all been run for 5 consecutive daily sessions and 1 member of each pair had been judged submissive. These 5 submissive animals were given septal lesions at the completion of their preoperative sessions. Following a two-week postoperative recovery period, testing was resumed. The animals were run for one 5 min session each day for 5 consecutive days.

exceeded the proportion displayed by their dominant normal opponents. Figure 4F presents the social investigatory category. During preoperative sessions, the dominant member of the pair consistently engaged in more of this activity (Z : 12.52, p < 0.001). Following surgery the submissive septals showed an increase in this category (Z = 16.30, p < 0.001), while their dominant opponents displayed less of this activity (Z = 8.45, p < 0.001). In the non-social categories there appeared to be less exploration in the first 2 postoperative sessions, but this difference disappeared in the last 3 sessions (see Fig. 4G). Hoarding, however, was markedly affected by the lesion. No hoarding was observed in the lesioned group even though more than 25 per cent of its behavior fell into this category during the last 2 preoperative sessions. The dominant normals continued to display a substantial amount of hoarding during all postoperative sessions.

Results The results of Experiment 2 are presented in Fig. 4. This figure compares the postoperative behavior of the septals with their preoperative performance as submissive normal animals. The data obtained from their dominant normal opponents is also presented. In preoperative testing, there was no significant difference between the members of the pairs in the proportion of their behavior devoted to fighting (see Fig. 4A). Similarly, in postoperative sessions the septals did not differ from their opponents in the proportion of fighting. However, both the septals and their opponents showed an overall increase in the amount of fighting during postoperative sessions (Z = 4.21, p < 0.001). Figure 4B presents the data on aggression. The septals, which had been submissive preoperatively, were no more aggressive than they had been as normals (Z = 0.54, p > 0.69) Their dominant normal opponents, however, became significantly more aggressive during postoperative testing (Z = 6.72, p < 0.001). In the submission category (Fig. 4C) no difference was observed between the preoperative and postoperative behavior of the submissive septals. The septals did, however, substantially increase their use of escape behavior (Fig. 4D) while, as was the case for submission, the behavior of their dominant normal opponents remained unchanged. In the defensive category (Fig. 4E) the septals decreased somewhat, but still

Conclusions The observation that septal ablation abolished hoarding behavior was made in Experiment 1 and confirmed in the present experiment. An increase in social investigatory behavior was also noted in Experiment 1 and confirmed in the present experiment. In Experiment 1, this effect was identified in a dominant septal. Because social investigatory activity involves the initiation of physical contact with an opponent, it might be considered inappropriate behavior for a submissive animal, yet the submissive septals in the present study engaged in as much activity as did the dominant septals of Experiment 1. Bunnell and Smith [6] have observed that some septal cotton rats persist in their approach behavior toward aggressive opponents to the point of being killed. The increase in

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social investigatory behavior observed in the 2 experiments reported here may be an example of the same phenomenon. A hoarding deficit and a change in social investigatory behavior were observed in both Experiments 1 and 2. They also appear to be unrelated to the social status of the septal animal. The remaining effects, however, seem to be dependent upon the social history of the organism. In Experiment 1, the lesion had a pronounced effect on the level of aggression displayed by the septal animal. In the present experiment, septal hamsters with a preoperative history of submissiveness showed no increase in aggression, and continued to behave submissively. The major change in the submissive behavior of these animals was in the escape category for which a significant increase was observed. This increase may have been secondary to increased aggression on the part of their dominant normal opponents, which, in turn, may have occurred in response to the increased social investigatory behavior of the submissive septals. EXPERIMENT 3

Experiments 1 and 2 demonstrated that septal ablation has a marked effect on the intraspecific aggressiveness and social behavior of the hamster. The effect o f septal ablation in the socially naive hamster was such that the animal became dominant in postoperative interactions with conspecific opponents. In socially experienced submissive animals, no such increase in aggressiveness was observed. Such animals may have been more submissive postoperatively as suggested by their disproportionate display of escape behavior. The present experiment was designed to serve two purposes. The first was to test the effect of the lesion in preoperatively dominant animals. In this instance it was predicted that the lesion would increase the aggressiveness of the animal. The second goal of the experiment was an attempt to further clarify the role of social history in the lesion effect. Before it could be shown that the nature of the lesion effect is controlled by the preoperative history of the animal, a possible confounding variable, the behavior of the opponent, had to be brought under experimental control. Dominant and submissive hamsters behave in distinctly different ways. During preoperative testing, the opponent of the animal to be lesioned provides a stimulus array characteristic of its social status. This same array is offered again in the postoperative sessions. if, for example, a septal animal had been submissive before surgery, its opponent would begin the postoperative sessions by responding in a manner characteristic of a dominant animal. The septal might retain its submissive status simply because its opponent behaved as though it were dominant and an argument against a relationship between lesion effect and social experience could be constructed. The present experiment was designed to control for this possibility. Fifty-six adult male hamsters were used in this study. All animals were housed and tested in the apparatus schematized in Fig. lB. The procedure was divided into 3 parts. Initially, all animals were assigned to matched weight pairs and run for one session a day for 5 consecutive days. At the completion of this procedure, 22 animals which were dominant and 11 which were submissive were selected to serve as subjects in the experiment. The sole purpose of this first step was to select these animals. Following their selection for the experiment, 11 of the dominant animals were randomly dected to receive septal lesions. Following a two-week post-operative recovery period, all animals were assigned to groups of 3. Each group consisted of a dominant septal, a dominant

normal, and a submissive animal which served as an opponent for the other two members of the group. Using a counterbalanced order, each dominant septal and each dominant normal were run one session a day against their mutual submissive opponent every other day to a total of 3 days. This procedure served to provide a direct comparison between the aggressive behavior of a dominant septal and a dominant normal since each interacted with the same submissive opponent. Furthermore, it served to give both dominant members of a group some measure of equivalent social experience. On the day following the completion of the procedure described above, the final procedure was begun. The submissive opponent for each group was dropped from the experiment and each dominant septal was run against the dominant normal from its group for one session a day for 5 consecutive days. The purpose of this procedure was to pair dominant septal animals against opponents with equivalent social status and experience. The opponents, in this instance, were dominant animals, the behavior of which would directly oppose any attempt by the septals to retain their social status. The only way in which they could do so was to continue to behave in terms of their social history, rather than the immediate stimulus array presented by their opponents. Results The results of Experiment 3 are summarized in Fig. 5. Only those response categories directly related to the present study are presented. Figures 5A through 5D summarize the data obtained from the 3 sessions in which both dominant septals and dominant normals opposed the same submissive opponent. Data of the submissive opponents are presented separately for sessions with a septal and again for sessions with an intact animal. Figures 5E through 5H present the data obtained from the 5 sessions in which the dominant septals and dominant normals opposed each other. Figure 5A presents the data on fighting. It indicates that septal-normal pairs consistently fought more than those pairs in which both animals were intact. Figure 5B shows that both the dominant septals and the dominant normals displayed more aggression than their mutual opponents. Of interest is the fact that while both dominant septals and dominant normals were opposing the same submissive group, the septats were consistently more aggressive ( Z - 19.26, p < 0.001). The proportion of aggressive responses was never less than 0.35 in the septal group while it did not exceed 0.19 in the dominant normal group. In the submission category (Fig. 5C) it was observed that the submissive animals displayed a larger proportion of submissive behavior when paired with septals than when opposing normal animals. Similarly, more escape behavior was used in sessions with septals than in sessions with normal animals. In the final part of Experiment 3, dominant septals opposed dominant normals. Figure 5E presents the data on fighting obtained from these pairings. The septals continued to fight at the same level as observed in earlier sessions with a submissive opponent. However, the normal animals increased their level of fighting to match that of the septals (see Fig. 5A). The septal animals continued to display a high level of aggression (Fig. 5F) although significantly less than in Fig. 5B (Z = 7.85, p < 0.001). Their normal opponents decreased their level of aggression (Z = 24.00, p < 0.001). The amount of aggression displayed by these animals did n o t differ significantly from that of the submissive opponents with which

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they were paired earlier in the experiment. Therefore, while both normals and septals showed decreased aggression, the normal animals showed a pattern similar to that seen in submissive hamsters. The data for submission are presented in Fig. 5G. The septals continued to show little or no submissive behavior, while their formerly dominant Opponents increased substantially in this category. Figure 5H supports the submission data. It indicates that approximately 25 per cent of all the behavior observed for the normal animals fell into the escape category, while the septals continued to show little or none of this behavior.

Conclusions The results of Experiment 3, together with those of Experiments 1 and 2 suggest that the effect of septal ablation on the social behavior of the hamster is to increase the aggressiveness of both socially naive and experienced dominant animals. If, however, the animal has had a preoperative history of submission this effect does not occur. Furthermore, the effect appears to be independent of the behavior of the opponent of the septal. Experiment 3 demonstrated that dominant septals remained dominant in interactions with experienced dominant opponents. Although the data are not reported here, submissive animals have been run using the procedure of Experiment 3. Both submissive septals and experienced submissive normals continued to behave submissively when paired with one another. The fact that neither the submissive septals nor submissive normals assumed a dominant status is not considered

surprising as our experience has been that submissive hamsters tend to remain so even though faced with new opponents. When experienced submissive animals are placed together they normally avoid one another and do not initiate fighting activity. Observations of the submissive septals indicate that the above is true for them as well.

EXPERIMENT 4

Experiment 4 was conducted in an attempt to further evaluate the role of social experience in determining the effect of a septal lesion. In previous experiments socially naive and dominant animals were found to be aggressive following septal ablation. This effect was not present in animals with a preoperative history of submission. In the present experiment the effect of the lesion was observed in animals with social experience, but without a history of either wins or losses in dominance fighting. This was possible because a small proportion of isolation-reared hamsters, although engaging in social activities, rarely show spontaneous aggression. The design of the study also permitted observation of the social interaction of septal animals matched with other septals. The 26 adult male hamsters used in the study were housed and tested in the dominance cage represented in Fig. lB. Preoperatively, each pair of animals was run one session a day for 3 consecutive days. At the completion of this testing, 3 randomly-selected groups were formed. One group of 5 pairs received no lesion. In a second group (4 pairs) one member of each pair received a septal lesion. In the third

86

SODEI'Z AND BUNNELL

group (4 pairs) both received septal lesions. Following a 2-week postoperative recovery period, all pairs were run one session a day for 5 consecutive days. Results

Preoperatively, the 13 pairs of hamsters engaged in very little social interaction. This was predictable as the animals in the present study were selected for their low level of aggressive activity. Consequently, the preoperative trials, afforded the animals a measure of social experience which did not include any decisive aggressive interaction. At the time of surgery, all animals, although socially experienced, had no social history of winning or losing. Figure 6 illustrates the effect of septal ablation in the socially experienced nonaggressive animals. In this figure, the scores obtained for the 4 aggressive behaviors in the response inventory ha~e been

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less aggressive septals (0.10) with that of their more aggressive septal opponents (0.01) indicated the less-aggressive animals were more submissive than their opponents (Z ~ 28.67, p < 0.001). This comparison supports the observation that the less-aggressive septals were, in fact, behaving as though they had become submissive. Conclusions

The present study demonstrated that preoperative social experience which does not include decisive aggressive interaction is of little significance in relation to the effect of septal ablation. It would appear that the effect of septal ablation in the hamster is to produce and maintain a high level of aggressiveness unless the animal experiences defeat either in preoperative trials or in postoperative trials. Several additional observations from the present study and other studies in the series should be noted. The display of aggressive behavior in the septal animal appears to be partially controlled by specific characteristics of its opponents. The septal hamster facing a normal opponent is more aggressive than a normal animal would be toward the same opponent; however, when a septal faces another septal, it becomes still more aggressive. The aggressiveness of the animal appears to vary according to the requirements of the situation. The level of aggression displayed by the septal is sufficient to defeat normal opponents. If however, the septal opposes another septal it may be defeated. Once defeated, the septal animal assumes a submissive status and behaves in a manner consistent with that role.

.05

0 r,,... 0..

DISCUSSION

NORMALS

SEPTALS

SEPTALS

AGGRESSION FIG. 6. Proportion of all observed responses which fell into the aggression category for normals ( n : 5 ) paired with normals, septals (n~--A) paired with normals, and septals (n~-~4) paired with septals in pre- and postoperative testing.

pooled to give a single value which is the percentage of all observed behaviors across all sessions which were in the aggression category. Figure 6A represents the normal pairs. These animals showed almost no aggression in preoperative testing, and following surgery their behavior remained unchanged. The septal animals (see Fig. 6B), however, present a different picture. When these animals were paired against the same normal opponents which they faced in preoperative trials, their aggression scores rose from less than 1 per cent to nearly 12 per cent. Not only were these animals more aggressive (Z = 29.30, p < 0.001), but in each case they dominated their opponents. The septal-septal group (Fig. 6C) is of special interest. These animals were also non-aggressive in preoperative trials. Following surgery, however, the animals engaged in vigorous aggressive interaction. The solid bar represents the aggression scores of those animals which emerged as dominant in each pair. Although the aggressive interaction in these pairs was quite vigorous, one member of each pair ultimately displayed more aggression (Z = 40.92, p < 0.001). A comparison of the submissive behavior of the

The results of the above experiments indicate that 3 kinds of changes occur in the behavior of the hamster following septal ablation. Two of these are independent of the preoperative history of the animal, the third depends upon its preoperative social experience. Following septal ablation, hoarding activity was reduced or absent in the male hamster. The effect was independent of the social history of the animal. Naive, experienced dominant, and experienced submissive hamsters all ceased to hoard or reduced the level of activity following surgery. Matalka [10] observed a similar result when he tested septal hamsters for hoarding in a 24-in. straight alley. Normal hamsters use the paper they hoard to construct nests in their home cages. Daily observation of the septal animals in the present study suggested that not only do such animals fail to hoard, they also fail to construct nests from available material. A second effect which occurred in all septals regardless of their social history was an increase in social investigatory activity. This behavior consisted of pawing and sniffing the animal with which they had been paired. An increase in aggression was observed in the present study, but unlike the changes in social investigatory behavior and hoarding the occurrence of the lesion effect was found to be dependent upon the preoperative social history of the animal. The present series of studies demonstrated that septal ablation in animals with a social history which did not include defeat by a conspecific opponent would increase aggressiveness as indicated by increased fighting, threat and attack behavior, and by the defeat of normal opponents. The nature of the increase in aggressiveness was such that septal animals consistently defeated even experienced dominant opponents. If,

SEPTAL ABLATION AND BEHAVIOR however, the septal had been defeated in preoperative testing, no increase in aggression occurred and following surgery the animal continued to behave submissively. The present study also demonstrated the modifiability of the effect. When septals were paired with other septals, they engaged in vigorous fighting. These fights were resolved, however, and 1 member of each pair became dominant and the other submissive. Furthermore, the amount of aggression displayed by a septal appeared to be at least partially determined by the behavior of its opponent. Septals opposing naive or experienced dominant normals displayed less aggression than did those opposing experienced submissive animals. Thus the lesion effect appeared to be modifiable both in terms of the fact that it could be cancelled if the septal animal were defeated, an event which only occurred if the animal was matched with another septal, and in terms of the fact that different levels of aggression were displayed against opponents with differing social histories. A fourth change, increased fighting, appeared to be secondary to changes in social investigatory and aggressive behaviors. In any pair in which at least one member was a septal, more fighting took place than in normal pairs. Several authors [1, 2] have recently reported an increased probability of fighting in septal rats subjected to painful electric shock. The data from the present study are similar, but, in contrast to the shock-elicited aggression situation, the increased fighting seen in our animals was not always a function of increased agressiveness by the septals. Although increased fighting was observed in pairs in which the septal animal was dominant and the aggressor, increased fighting also occurred in those pairs in which the septal was submissive and the object of aggression. In these pairs, fighting probably occurred because the persistent social investigatory behavior of the submissive septals elicited aggression from their dominant normal opponents. In the rat, septal ablation produces a transient change in behavior known under a variety of names such as "septal rage", "hyperemotionality", or "septal hyperirritability". All of the lesioned animals in experiments one and two were rated for this phenomenon both pre- and postoperatively using a modification of the King scale [9] developed for use with the rat. The data from those animals along with those of 8 other septal animals has been presented elsewhere [15]. No preand postoperative difference could be found in the behavior of these animals, nor has any difference ever been noted in any septal hamster in these and other experiments in our laboratory. It seems likely that the effects obtained in the present study were unrelated to the septal rage phenomenon observed in the rat. Many of the behavioral effects of septal ablation can be subsumed under a model based upon "response disinhibition" [11]. While both the increases in aggressive and social investigatory behavior observed in the present study are consistent with such a model, some other concept of septal function appears to be necessary to account for all of the data. Hoarding may account for as much as 35 per cent of the behavior of normal hamsters observed in the testing situation used in the present study. The presentation of nesting materials or food pellets is sufficient to elicit this response. However,

87 septal animals were observed to hoard infrequently, or not at all. In the presence of a powerful stimulus, such as nesting material, one would predict an increase in hoarding if the hamster suffered for some general deficit related to an inability to inhibit established responses. Similarly, the absence of further aggression on the part of a defeated septal suggests that the animal is capable of withholding aggressive responses. The data from the present experiment have been examined in terms of the sequences of individual behavioral acts used by both normals and septals. A description of the sequences shown by dominant and submissive normal hamsters is available elsewhere [7]. Septal hamsters do not appear to be qualitatively different from normals in terms of intra-animal sequences of social behavior. All of the behavioral chains seen in normals are present in septals, and no new sequences are observed in the lesioned animals. Such changes as do appear are in the frequency with which certain sequences are used, and these appear to be secondary to the increased frequency of occurrence of social investigatory behaviors seen in all septals, and to the increased aggressive responses seen in preoperatively socially naive septals. More recent work from our laboratory [4, 14] indicates that the role of the septum in the 3 kinds of behavioral changes seen in the present study may be attributable to the participation of the septal nuclei in at least 2, and probably more, separate functional circuits. For example, bilateral lesions of the amygdala prevent the appearance of increased aggressive behavior seen in preoperatively socially naive septals, but have no effect on the increased social investigatory behavior or the reduction in hoarding activity produced by the septal lesions. The great variety of septal lesion effects [16], and the difficulty that is encountered in trying to subsume all of these effects under any one of the unitary concepts of behavioral deficit, makes the value of such uniprocess interpretations problematical. If there is any single concept under which the present results may be subsumed, it can best be characterized as a diminished responsiveness to the stimuli which normally serve to modify and control the behavior of the intact animal. Thus, the failure of the septal to hoard, the persistent approaches to aggressive opponents, and the continued aggressiveness in the presence of submissive behavior by an opponent, all indicate a change in the significance of stimuli involved in the regulation of neural response mechanisms. As a working hypothesis, such an interpretation suggests that more attention needs to be paid to such matters as the identification of critical stimuli, the importance of the different senses in directing these complex but rather highly stereotyped patterns of behavior, and the relative importance of endogenous and exogenous stimuli in the control of each of the behaviors under investigation. A change in the responsiveness of the septal hamster to normally significant stimuli may account for a failure to respond, as in the case of hoarding and nesting when such stimuli normally serve to elicit a response, or for an augmentation of response, as in the case of social investigatory and (with appropriate preoperative experience) aggressive behaviors, when such cues may normally provide stimuli leading to response suppression or inhibition.

88

SODEIZ AND BUNNISI. REFERENCES

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