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Dorsolateral frontal lobe lesions and behavior in the macaque: Dissociation of threat and aggression
Physiology & Behavior, Vol. 17, pp. 209--213. Pergamon Press and Brain Research Publ., 1976. Printed in the U.S.A.
Dorsolateral Frontal Lobe Lesions and Behavior in the Macaque: Dissociation of Threat and Aggression MICHAEL H. MILLER
Department o f Psychiatry, CMDNJ-Rutgers Medical School, Piscataway, N J 08854 (Received 30 May 1975) MILLER, M. H. Dorsolateral frontal lobe lesions and behavior in the macaque: dissociation of threat and aggression. PHYSIOL. BEHAV. 17(2) 209-213, 1976. -- Eight male juvenile rhesus monkeys (Macao Mulatta) were housed in an enclosure and observed for a period of 13 months. During that time, each animal sustained dorsolateral frontal lobe resection. Two monkeys were removed from the group and one operated until four were lesioned; the remaining four animals were then lesioned en bloc. Observations on the group were analyzed at three points: one monkey lesioned, four lesioned, and all eight lesioned. Several social behaviors were recorded over the course of the experiment and both individual and group levels compared over observation periods. Although preopreative relationships, levels of affiliative interaction, and, for the most part, order of dominance remained stable after surgery, marked changes in aggression and threat behavior were seen. The diminution in occurrence of threats and concomitant increase in aggression are viewed as supportive of a model of frontal lobe function incorporating stimulus processing properties and lack of inhibition. This theoretical position is used to explain complementary results found in both the laboratory and field settings. Dorsolateral frontal lobe lesions
Socialbehavior
Aggression Rhesus monkeys
TRADITIONALLY, disorders resulting from frontal lobe resection have been studied in individually housed laboratory animals. In the continuing effort to explain the nature of frontal lobe function, studies have shifted from individually caged animals to observations of lesioned animals in a social setting. In a laboratory setting, dorsolateral frontal ablation was reported to have caused a diminution of submissive behavior and an increase in aggression directed toward higher status monkeys [1,2]. Although ultimately, this resulted in a greater intensity of downward aggression throughout the hierarchy, it interfered with the maintenance of group stability because of the inability of the operates to adjust to their relative position within the social structure. Stumptail macaques housed in a room sized enclosure received orbitofrontal lesions with a resultant fall in dominance seen in several monkeys. They also showed diminished amounts of aggression and positive interaction as well [7]. In a similarly composed group sustaining dorsolateral lesions, a change in the hierarchial structure was seen after some time postoperatively and accompanied by increased aggression and hyperactivity [4]. Tliese findings taken together indicate a possible dissociation of function in social behavior between these two areas of frontal cortex. Recently, Myers, Swett and Miller studied frontal lobe lesioned animals in a semi free ranging setting on Cayo Santiago, an island off the coast of Puerto Rico [6]. In this setting, frontal lobectomy was shown to have marked
effects on the social behavior of the free ranging macaques. Lesioned animals failed to rejoin their social group. They were seen to run through the group and failed to survive after more than a week in the solitary state. In view of the diminished social stability and lack of social affinity following frontal lesions, an inquiry into the nature of the mechanisms underlying such change is needed. If the disturbance caused by frontal lobe resection is such that a rhesus monkey sustaining such a lesion fails to rejoin his social troop, what might be some of the factors that result in the tendency to isolate himself spatially from other animals in a field situation? Since animals that became solitary in a field setting were difficult to observe, perhaps a more confining situation would enable observers to assess postoperative behavior. If the animals were placed within limited spatial confines, day-to-day scrutiny might reveal subtle changes not evident in a larger setting. Additionally, by studying a homogenous group of monkeys, changes in levels of interactions, both agonisitic and associative could be used to ascertain lesion effects upon group processes and to compare their interactions with observations in a field setting. METHOD
Animals Eight feral-born male juvenile rhesus monkeys (weighing between 2 and 4 kg) were grouped for the first time together for this study. 209
210
Apparatus All observations were carried out with the monkeys housed together in an 8 × 6 ft wire mesh enclosure which was situated within a larger room. The experimenter viewed the monkeys through a 3 × 5 ft Plexiglas window in one side of the enclosure.
Procedure Observations were divided into three periods, each divided into two 10-hr blocks. Six months before the initial grouping, monkey No. 8 sustained a frontal lobe lesion. After 60 days together, during which the social patterns and group structure were allowed to consolidate, observations were initiated. The first two blocks of behavior were recorded (Period 1), then a surgical schedule was imposed as follows: two animals were removed from the group and one subjected to bilateral resection of dorsolateral frontal cortex. The other was removed as a control for changes in social rank and to equalize the amount of time out of the group for all monkeys. The second observation period of two 10-hr data blocks, followed after four of the eight monkeys were operated. Then the animals were caged separately and the remaining four monkeys lesioned en bloc. After postoperative recovery, the group was re-formed and the third observation period of two 10-hr blocks followed. During this time, all eight monkeys had sustained cortical resections. We collected data at least 2 hr after the morning feeding at approximately the same time each day. In order to avoid over-concentrating observation periods, we used daily sessions of 30 min, with an effort to accumulate at least 3 hr each week. Behavior. Observation consisted of recording the ongoing activity each animal manifested in the group. (1) Joins: When the animals sat down next to or walked alongside another monkey. (2) Joined: When another animal sat next to or walked along with the monkey. (3) Grooms: When the animal picked at the skin or ran his hands through the fur of another. (4)Groomed: When another animal picked at the skin or ran his hands through the fur of the monkey. (5)Threatens: When the animal made facial or postural displays toward another animal which usually resulted in fight-flight, or submissive displays on the part of the threatened animal. (6) Threatened: When another animal made these displays towards the monkey. (7) Aggress: Overt, biting, hitting or chasing another monkey. (8) Aggressed: When another animal behaved similarly toward the monkey. Time spent together in actual physical contact was scored as well. Behavior was recorded in terms of incidence of occurrence except for grooming and together which were measured in terms of duration (min). Hierarchial dominance was determined from observations of the direction of aggression and threats and the resultant submissive behavior on the part of the subordinate monkey. Surgery. All monkeys were operated using aseptic precautions and anesthetized with a combination of Nembutal and Sernalyn. Bilateral lesions were made in one stage by turning a transverse bone flap and revealing both dorsolateral surfaces simultaneously. Cortex anterior to the arcuate sulcus was aspirated. Special effort was made to remove cortex along the banks and depths of the principal sulcus forward to the frontal pole. Postoperative care included administration of 500,000 units of Penicillin and
MILLER normal saline as needed. Dermal sutures were removed within a week. Histology. At the completion of the study, all animals were killed with an overdose of Nembutal and perfused with saline and 10% solution of Formalin. The brains were embedded in celloidin and serially sectioned at 50 u. Every 20th section was mounted and stained with cresyl violet stain to reveal the extent of cortical damage and resultant cellular degeneration in the dorsal medial nucleus of the thalamus. The extent of the lesions were drawn using a photographic enlarger to project the stained and mounted brain sections. These are portrayed in Fig. 1.
RESULTS
After each operated monkey was returned to the group, definite behavioral changes were observed. The incessant hyperactivity of the recent operate was tolerated to a point by others in the social group. However, after several minutes of rapid and repetitive pacing by the recent operate, others within the group seemed to lose patience and agonism toward the offender would ensue. Usually, other operates would abruptly aggress without warning. Normal monkeys often made threatening gestures before attacking when they did so, but operates appeared to manifest mask-like faces even during aggression. Nevertheless, aggression occurred in the appropriate direction (downward) within the hierarchy and operates always submitted to a more dominant monkey. Aggression increased over the course of the three observation periods (Table 1). Between the first and third periods, levels of aggression tripled. Contrary to the Brody and Rosvold study [ 1 ], much of the increased aggression in the present experiment was seen in higher ranking monkeys. This may represent attempts by the monkeys to maintain dominance, as the aggression continued to be appropriately directed and the hierarchical order remained much the same. Monkey No. 8 rose in rank and monkey No. 3 fell in dominance. Each changed two position. Aggression levels seen in Table I reflect these position changes in the hierarchy. The preoperative levels of aggression in Period 1 were statistically compared with aggression observed in Period 3 when all animals had been operated. Differences for each monkey were matched with its rank in the dominance hierarchy. Increases in aggression were directly related to dominance rank (r s = 0.65; p<0.05; n = 8; Spearman rank Correlation). Threatening behavior diminished over the course of observation (Table 2). Monkeys numbered 2 and 5 were the only ones to show an increase in threatening postoperatively; even though, in the next period, these levels declined below their initial values. Inspection of Fig. 2 also reveals the marked decrease in threat for the group as a whole over the course of the study. Changes in this behavior were most prominent in these monkeys exhibiting initially higher levels. Those animals who threatened little from the beginning could only reduce its occurrence accordingly. Because of this we compared differences in threat behavior, before and after surgery, with rank in the dominance hierarchy. Decreases in this behavior varied directly with hierarchical position, ie., high ranking monkeys showed greater differences in threatening after surgery than
DORSOLATERAL FRONTAL LOBE LESIONS
1
211 TABLE 1
5
AGGRESSION: INCIDENCE OF AGGRESSION FOR EACH ANIMAL PER OBSERVATION PERIOD
2
6
Period 1
Period 2
Period 3
MONKEY No. 1 2 3 4 5 6 7 8 Group mean # = X normal monkeys =
11.0 7.0 9.0 3.0 9.0 8.0 2.0 0.0 6.1 7
45.6 30.7 12.0 19.7 19.0 4.3 0 1.6 16.6 15.5
X operated monkeys =
0
17.8
25.5 44.5 6.5 40.0 20.5 0.5 1.5 9.0 18.5 8.5 recently operated 28.5 previously operated
D
3
7
The bold face numbers indicate surgery before period. TABLE 2 THREATENS--TOTAL FOR EACH ANIMAL PER OBSERVATION PERIOD
4
FIG.
8
Extent of lesions. Stippled areas indicate some cortex remaining.
did those low in d o m i n a n c e (r s = 0.70; p < 0 . 0 5 ; n = 8; Spearman rank Correlation). Mean numbers of threats for each observation period shows that normal m o n k e y s t h r e a t e n e d m o r e o f t e n than did frontally lesioned monkeys. D r a m a t i c decreases in such behavior were seen in the third period after all animals had sustained lesions. The m e a n level had d r o p p e d to 2 threats (per animal) for that period. By contrast, the first observation period revealed a m e a n level of 15.7 threats per normal m o n k e y (Table 2). T h r o u g h o u t the e x p e r i m e n t , M o n k e y No. 8 showed very low threat levels even though u l t i m a t e l y he rose in rank f r o m eighth to fifth in dominance. M o n k e y s t e n d e d to choose the same grooming, t o g e t h e r and joining partners t h r o u g h o u t the three observation periods, i n d e p e n d e n t of intervention by brain lesions (Fig. 3).
MONKEY No. 1 2 3 4 5 6 7 8 X for group= X for normal monkeys=
X operated monkeys =
Period 1
Period 2
Period 3
27.0 7.0 11.0 43.0 3.0 15.0 4.0 0.0 13.8
52.3 9.6 9.3 9.8 4.0 1.2 0.6 0.0 10.9
1.5 5.5 1.0 3.5 2.5 0.0 0.5 1.5 2.0
15.7
15.9
0
5.6
0.75 recently operated 3.25 Previously operated
The bold face numbers indicate surgery before period. This figure illustrates the relative constancy of nonagonistic behaviors over the course of the experiment. Joins, grooms, play and together, representing affiliative behavior, changed little across observation periods. However, t h e y did increase slightly during the second period w h e n four of eight m o n k e y s were operated. The third period when all m o n k e y s had been operated, showed a d i m i n u t i o n in these behaviors and a return to levels observed in Period 1. DISCUSSION The results of this experiment demonstrate some specific
212
MILLER
THREAT
20 z16 I.l.I ~ 0 14 I.iJ 0::12 LI-
-
~
AGGRESSION
I0
8 6 4 2
!Ii':~1
ii
!i;
7 NORMALS) I OPERATE
(~ NORMALS / OPERATES/
I
2
(8 OPERATES)
3
OBSERVATION PERIOD FIG. 2. Mean incidence of threat and aggression seen in the group of 8 macaques compared over observation periods. 75.
[] JOINS [ ] TOGETHER
• PLAYS
0. ¢.~
[] GROOM
• SELF-GROOM
z 45" nr"
o
30-
i,i n," It..
15-
_I, I
2
3
OBSERVATION PERIOD
FIG. 3. Non-agonistic behaviors compared over observation periods. effects of resection of dorsolateral frontal cortex on a group of male juvenile rhesus monkeys small enclosed area. The usual increase in locomotor pacing and hyperactivity was seen in each monkey within a few days of surgery. Nevertheless, with all monkeys operated, after a period of several months, they were able to habituate to the presence of the observer and hyperactivity was noticed to decrease somewhat. After introducing an operate to the social group, hyperactivity and confusion usually ensued. Although this condition became quite extreme after several in the group were operated and hyperreactive, we observed little change in the hierarchy. A recently operated monkey was able to re-establish his position in the hierarchy. This is consistent with the stable hierarchy of the males observed in a
heterosexual group of stump-tailed macaques following dorsolateral ablations [4]. In contrast, in the aforementioned study, several females fell in rank after surgery. In the present study, operated monkeys continued to maintain similar relationships with others vis ~ vis levels of affiliative responses such as grooming, joining, playing and time together. In fact, individual partner preferences among operates remained constant after surgery. Even when a change in dominance occurred as with No. 8, in his new position, his partner choices were the same as in the previous observation periods. A sharp decrease in group levels of aggression was observed over the course of this study. The rise in levels of aggression were usually seen following ablation and most often in monkeys of middle and high social rank. That these sharp increases in aggression were coupled with a dramatic diminution of threat gestures marks a qualitative change in the behavior of operates. Prior to surgery, threats were part of a sequence involving a visual display and various submissive gestures that might forestall aggression; postoperatively this sequence was eliminated. Aggression occurred abruptly and without warning and was followed by a simple displacement of aggression to another monkey or a fleeing response. In both attacker and recipient, the marked absence of facial stare or head bob in the former, and facial grimace or lip smacking in the latter were noted. These findings are consistent with those of Myers who found a mild weakness in facial expression following lesions of frontal cortex [ 5 ]. After all eight monkeys had been operated, the group cage became a blur of activity. Heightened activity levels were seen in all operates and over the course of the study, diminished only slightly. The presence of stereotyped pacing, however, did not interfere with affiliative behavior• In contrast, lesions of orbitofrontal cortex have produced hypoactive animals that show diminished amounts of affiliative as well as agonistic behavior [7,8].
DORSOLATERAL FRONTAL LOBE LESIONS
213
The increased aggression observed in the present experiment had not been seen in field situations where the operate was able to withdraw from contact with other monkeys [6]. In a field setting, a released operate may be confused by the complex array of stimuli that are presented by an awaiting social group. Within this context, he may be unable to separate stimuli and inhibit the response tendency to flee. Withdrawal to a noninteractive, solitary situation results. Perhaps within the confines of the laboratory enclosure, the operated monkey is forced into contact with others and is unable to express the proper signals to avoid direct attack. In the limited space of the enclosure, these displays are necessary to avoid such contacts and, frontal animals, unable to express them, cannot avoid these encounters and aggress more. However, by the same token, affiliative behavior is maintained (Fig. 3) in the present setting. This indicates that frontally lesioned monkeys in a restricted spatial environment can maintain affiliations but, at the same time, change agonistic responses. In a study carried out in a group of stump-tailed macaques sustaining dorsolateral frontal lesions, social
affiliative behavior in an expanded spatial context (1/2 acre) is being compared to behavior of the same group obseryed in a laboratory enclosure. Preliminary results indicate that there is a relative increase in spatial distancing by operates from the core group in the 1/2 acre enclosure. A theoretical model of frontal lobe function incorporating attention and stimulus processing proposed by Konorski and Lawicka helps to account for the inability of the operate to sort out incoming information and resort to aggression in the face of the resultant confusion [3]. We have seen in the operated monkey the ability to maintain affiliative relations with other group members and to interact with them, (e.g. grooming, joining and playing). However, they no longer utilize facial expression and resort to direct aggression. Perhaps because of a perceptualcognitive deficit, the frontal monkey is unable to perceive and/or react to complex stimulus situations nor to inhibit certain responses to these stimuli. In conclusion, a model of frontal lobe damage that suggests difficulty in stimulus processing and failure of inhibitory mechanisms that are exacerbated by the hyperactive state may serve to explain the results of this study.
REFERENCES 1. Brody, E. G. and H. E. Rosvold. Influence of prefrontal lobotomy on social interaction in a monkey group. Psychosom. Med. 14: 406-415, 1952. 2. Deets, A. C., H. F. Harlow, S. D. Singh and A. J. Blomquist. Effects of bilateral lesions of the frontal granular cortex on the social behavior of rhesus monkeys. J. comp. physiol. Psychol. 72: 452-461, 1970. 3. Konorski, J. and W. Lawieka. Analysis of errors by prefrontal animals on the delayed response test. In: The Frontal Granular Cortex and Behavior, edited by J. M. Warren and K. Akert. New York: McGraw-Hill,1964, pp. 271-294. 4. Mass, R. The effects of dorsolateral ~rontal ablations on social behavior of a caged group of eleven stumptail macaques. Doctoral dissertation, Rutgers UniversityGraduate School, Department of Psychology, 1973.
5. Myers, R. E. Neurology of social communication in primates. Proc. of 2nd International Congr. of Primatology at Yerkes Reg. Primate Ctr. Basel: Karger, 1968. 6. Myers, R. E., C. Swett and M. H. Miller. Loss of social group affinity following prefrontal lesoins in free-ranging macaques. Brain Res. 64: 257-269, 1973. 7. Notkin, E. The effects of orbital-frontal lesions on the social behavior of the caged stump-tailed macaque (Macaca speciosa). Master's thesis, Rutgers University Graduate School, Department of Psychology, 1972. 8. Snyder, D. R. Fall from social dominance following orbital frontal ablation in monkeys. Proceedings 78th Annual Convention, APA, 1970.
Dorsolateral Frontal Lobe Lesions and Behavior in the Macaque: Dissociation of Threat and Aggression MICHAEL H. MILLER
Department o f Psychiatry, CMDNJ-Rutgers Medical School, Piscataway, N J 08854 (Received 30 May 1975) MILLER, M. H. Dorsolateral frontal lobe lesions and behavior in the macaque: dissociation of threat and aggression. PHYSIOL. BEHAV. 17(2) 209-213, 1976. -- Eight male juvenile rhesus monkeys (Macao Mulatta) were housed in an enclosure and observed for a period of 13 months. During that time, each animal sustained dorsolateral frontal lobe resection. Two monkeys were removed from the group and one operated until four were lesioned; the remaining four animals were then lesioned en bloc. Observations on the group were analyzed at three points: one monkey lesioned, four lesioned, and all eight lesioned. Several social behaviors were recorded over the course of the experiment and both individual and group levels compared over observation periods. Although preopreative relationships, levels of affiliative interaction, and, for the most part, order of dominance remained stable after surgery, marked changes in aggression and threat behavior were seen. The diminution in occurrence of threats and concomitant increase in aggression are viewed as supportive of a model of frontal lobe function incorporating stimulus processing properties and lack of inhibition. This theoretical position is used to explain complementary results found in both the laboratory and field settings. Dorsolateral frontal lobe lesions
Socialbehavior
Aggression Rhesus monkeys
TRADITIONALLY, disorders resulting from frontal lobe resection have been studied in individually housed laboratory animals. In the continuing effort to explain the nature of frontal lobe function, studies have shifted from individually caged animals to observations of lesioned animals in a social setting. In a laboratory setting, dorsolateral frontal ablation was reported to have caused a diminution of submissive behavior and an increase in aggression directed toward higher status monkeys [1,2]. Although ultimately, this resulted in a greater intensity of downward aggression throughout the hierarchy, it interfered with the maintenance of group stability because of the inability of the operates to adjust to their relative position within the social structure. Stumptail macaques housed in a room sized enclosure received orbitofrontal lesions with a resultant fall in dominance seen in several monkeys. They also showed diminished amounts of aggression and positive interaction as well [7]. In a similarly composed group sustaining dorsolateral lesions, a change in the hierarchial structure was seen after some time postoperatively and accompanied by increased aggression and hyperactivity [4]. Tliese findings taken together indicate a possible dissociation of function in social behavior between these two areas of frontal cortex. Recently, Myers, Swett and Miller studied frontal lobe lesioned animals in a semi free ranging setting on Cayo Santiago, an island off the coast of Puerto Rico [6]. In this setting, frontal lobectomy was shown to have marked
effects on the social behavior of the free ranging macaques. Lesioned animals failed to rejoin their social group. They were seen to run through the group and failed to survive after more than a week in the solitary state. In view of the diminished social stability and lack of social affinity following frontal lesions, an inquiry into the nature of the mechanisms underlying such change is needed. If the disturbance caused by frontal lobe resection is such that a rhesus monkey sustaining such a lesion fails to rejoin his social troop, what might be some of the factors that result in the tendency to isolate himself spatially from other animals in a field situation? Since animals that became solitary in a field setting were difficult to observe, perhaps a more confining situation would enable observers to assess postoperative behavior. If the animals were placed within limited spatial confines, day-to-day scrutiny might reveal subtle changes not evident in a larger setting. Additionally, by studying a homogenous group of monkeys, changes in levels of interactions, both agonisitic and associative could be used to ascertain lesion effects upon group processes and to compare their interactions with observations in a field setting. METHOD
Animals Eight feral-born male juvenile rhesus monkeys (weighing between 2 and 4 kg) were grouped for the first time together for this study. 209
210
Apparatus All observations were carried out with the monkeys housed together in an 8 × 6 ft wire mesh enclosure which was situated within a larger room. The experimenter viewed the monkeys through a 3 × 5 ft Plexiglas window in one side of the enclosure.
Procedure Observations were divided into three periods, each divided into two 10-hr blocks. Six months before the initial grouping, monkey No. 8 sustained a frontal lobe lesion. After 60 days together, during which the social patterns and group structure were allowed to consolidate, observations were initiated. The first two blocks of behavior were recorded (Period 1), then a surgical schedule was imposed as follows: two animals were removed from the group and one subjected to bilateral resection of dorsolateral frontal cortex. The other was removed as a control for changes in social rank and to equalize the amount of time out of the group for all monkeys. The second observation period of two 10-hr data blocks, followed after four of the eight monkeys were operated. Then the animals were caged separately and the remaining four monkeys lesioned en bloc. After postoperative recovery, the group was re-formed and the third observation period of two 10-hr blocks followed. During this time, all eight monkeys had sustained cortical resections. We collected data at least 2 hr after the morning feeding at approximately the same time each day. In order to avoid over-concentrating observation periods, we used daily sessions of 30 min, with an effort to accumulate at least 3 hr each week. Behavior. Observation consisted of recording the ongoing activity each animal manifested in the group. (1) Joins: When the animals sat down next to or walked alongside another monkey. (2) Joined: When another animal sat next to or walked along with the monkey. (3) Grooms: When the animal picked at the skin or ran his hands through the fur of another. (4)Groomed: When another animal picked at the skin or ran his hands through the fur of the monkey. (5)Threatens: When the animal made facial or postural displays toward another animal which usually resulted in fight-flight, or submissive displays on the part of the threatened animal. (6) Threatened: When another animal made these displays towards the monkey. (7) Aggress: Overt, biting, hitting or chasing another monkey. (8) Aggressed: When another animal behaved similarly toward the monkey. Time spent together in actual physical contact was scored as well. Behavior was recorded in terms of incidence of occurrence except for grooming and together which were measured in terms of duration (min). Hierarchial dominance was determined from observations of the direction of aggression and threats and the resultant submissive behavior on the part of the subordinate monkey. Surgery. All monkeys were operated using aseptic precautions and anesthetized with a combination of Nembutal and Sernalyn. Bilateral lesions were made in one stage by turning a transverse bone flap and revealing both dorsolateral surfaces simultaneously. Cortex anterior to the arcuate sulcus was aspirated. Special effort was made to remove cortex along the banks and depths of the principal sulcus forward to the frontal pole. Postoperative care included administration of 500,000 units of Penicillin and
MILLER normal saline as needed. Dermal sutures were removed within a week. Histology. At the completion of the study, all animals were killed with an overdose of Nembutal and perfused with saline and 10% solution of Formalin. The brains were embedded in celloidin and serially sectioned at 50 u. Every 20th section was mounted and stained with cresyl violet stain to reveal the extent of cortical damage and resultant cellular degeneration in the dorsal medial nucleus of the thalamus. The extent of the lesions were drawn using a photographic enlarger to project the stained and mounted brain sections. These are portrayed in Fig. 1.
RESULTS
After each operated monkey was returned to the group, definite behavioral changes were observed. The incessant hyperactivity of the recent operate was tolerated to a point by others in the social group. However, after several minutes of rapid and repetitive pacing by the recent operate, others within the group seemed to lose patience and agonism toward the offender would ensue. Usually, other operates would abruptly aggress without warning. Normal monkeys often made threatening gestures before attacking when they did so, but operates appeared to manifest mask-like faces even during aggression. Nevertheless, aggression occurred in the appropriate direction (downward) within the hierarchy and operates always submitted to a more dominant monkey. Aggression increased over the course of the three observation periods (Table 1). Between the first and third periods, levels of aggression tripled. Contrary to the Brody and Rosvold study [ 1 ], much of the increased aggression in the present experiment was seen in higher ranking monkeys. This may represent attempts by the monkeys to maintain dominance, as the aggression continued to be appropriately directed and the hierarchical order remained much the same. Monkey No. 8 rose in rank and monkey No. 3 fell in dominance. Each changed two position. Aggression levels seen in Table I reflect these position changes in the hierarchy. The preoperative levels of aggression in Period 1 were statistically compared with aggression observed in Period 3 when all animals had been operated. Differences for each monkey were matched with its rank in the dominance hierarchy. Increases in aggression were directly related to dominance rank (r s = 0.65; p<0.05; n = 8; Spearman rank Correlation). Threatening behavior diminished over the course of observation (Table 2). Monkeys numbered 2 and 5 were the only ones to show an increase in threatening postoperatively; even though, in the next period, these levels declined below their initial values. Inspection of Fig. 2 also reveals the marked decrease in threat for the group as a whole over the course of the study. Changes in this behavior were most prominent in these monkeys exhibiting initially higher levels. Those animals who threatened little from the beginning could only reduce its occurrence accordingly. Because of this we compared differences in threat behavior, before and after surgery, with rank in the dominance hierarchy. Decreases in this behavior varied directly with hierarchical position, ie., high ranking monkeys showed greater differences in threatening after surgery than
DORSOLATERAL FRONTAL LOBE LESIONS
1
211 TABLE 1
5
AGGRESSION: INCIDENCE OF AGGRESSION FOR EACH ANIMAL PER OBSERVATION PERIOD
2
6
Period 1
Period 2
Period 3
MONKEY No. 1 2 3 4 5 6 7 8 Group mean # = X normal monkeys =
11.0 7.0 9.0 3.0 9.0 8.0 2.0 0.0 6.1 7
45.6 30.7 12.0 19.7 19.0 4.3 0 1.6 16.6 15.5
X operated monkeys =
0
17.8
25.5 44.5 6.5 40.0 20.5 0.5 1.5 9.0 18.5 8.5 recently operated 28.5 previously operated
D
3
7
The bold face numbers indicate surgery before period. TABLE 2 THREATENS--TOTAL FOR EACH ANIMAL PER OBSERVATION PERIOD
4
FIG.
8
Extent of lesions. Stippled areas indicate some cortex remaining.
did those low in d o m i n a n c e (r s = 0.70; p < 0 . 0 5 ; n = 8; Spearman rank Correlation). Mean numbers of threats for each observation period shows that normal m o n k e y s t h r e a t e n e d m o r e o f t e n than did frontally lesioned monkeys. D r a m a t i c decreases in such behavior were seen in the third period after all animals had sustained lesions. The m e a n level had d r o p p e d to 2 threats (per animal) for that period. By contrast, the first observation period revealed a m e a n level of 15.7 threats per normal m o n k e y (Table 2). T h r o u g h o u t the e x p e r i m e n t , M o n k e y No. 8 showed very low threat levels even though u l t i m a t e l y he rose in rank f r o m eighth to fifth in dominance. M o n k e y s t e n d e d to choose the same grooming, t o g e t h e r and joining partners t h r o u g h o u t the three observation periods, i n d e p e n d e n t of intervention by brain lesions (Fig. 3).
MONKEY No. 1 2 3 4 5 6 7 8 X for group= X for normal monkeys=
X operated monkeys =
Period 1
Period 2
Period 3
27.0 7.0 11.0 43.0 3.0 15.0 4.0 0.0 13.8
52.3 9.6 9.3 9.8 4.0 1.2 0.6 0.0 10.9
1.5 5.5 1.0 3.5 2.5 0.0 0.5 1.5 2.0
15.7
15.9
0
5.6
0.75 recently operated 3.25 Previously operated
The bold face numbers indicate surgery before period. This figure illustrates the relative constancy of nonagonistic behaviors over the course of the experiment. Joins, grooms, play and together, representing affiliative behavior, changed little across observation periods. However, t h e y did increase slightly during the second period w h e n four of eight m o n k e y s were operated. The third period when all m o n k e y s had been operated, showed a d i m i n u t i o n in these behaviors and a return to levels observed in Period 1. DISCUSSION The results of this experiment demonstrate some specific
212
MILLER
THREAT
20 z16 I.l.I ~ 0 14 I.iJ 0::12 LI-
-
~
AGGRESSION
I0
8 6 4 2
!Ii':~1
ii
!i;
7 NORMALS) I OPERATE
(~ NORMALS / OPERATES/
I
2
(8 OPERATES)
3
OBSERVATION PERIOD FIG. 2. Mean incidence of threat and aggression seen in the group of 8 macaques compared over observation periods. 75.
[] JOINS [ ] TOGETHER
• PLAYS
0. ¢.~
[] GROOM
• SELF-GROOM
z 45" nr"
o
30-
i,i n," It..
15-
_I, I
2
3
OBSERVATION PERIOD
FIG. 3. Non-agonistic behaviors compared over observation periods. effects of resection of dorsolateral frontal cortex on a group of male juvenile rhesus monkeys small enclosed area. The usual increase in locomotor pacing and hyperactivity was seen in each monkey within a few days of surgery. Nevertheless, with all monkeys operated, after a period of several months, they were able to habituate to the presence of the observer and hyperactivity was noticed to decrease somewhat. After introducing an operate to the social group, hyperactivity and confusion usually ensued. Although this condition became quite extreme after several in the group were operated and hyperreactive, we observed little change in the hierarchy. A recently operated monkey was able to re-establish his position in the hierarchy. This is consistent with the stable hierarchy of the males observed in a
heterosexual group of stump-tailed macaques following dorsolateral ablations [4]. In contrast, in the aforementioned study, several females fell in rank after surgery. In the present study, operated monkeys continued to maintain similar relationships with others vis ~ vis levels of affiliative responses such as grooming, joining, playing and time together. In fact, individual partner preferences among operates remained constant after surgery. Even when a change in dominance occurred as with No. 8, in his new position, his partner choices were the same as in the previous observation periods. A sharp decrease in group levels of aggression was observed over the course of this study. The rise in levels of aggression were usually seen following ablation and most often in monkeys of middle and high social rank. That these sharp increases in aggression were coupled with a dramatic diminution of threat gestures marks a qualitative change in the behavior of operates. Prior to surgery, threats were part of a sequence involving a visual display and various submissive gestures that might forestall aggression; postoperatively this sequence was eliminated. Aggression occurred abruptly and without warning and was followed by a simple displacement of aggression to another monkey or a fleeing response. In both attacker and recipient, the marked absence of facial stare or head bob in the former, and facial grimace or lip smacking in the latter were noted. These findings are consistent with those of Myers who found a mild weakness in facial expression following lesions of frontal cortex [ 5 ]. After all eight monkeys had been operated, the group cage became a blur of activity. Heightened activity levels were seen in all operates and over the course of the study, diminished only slightly. The presence of stereotyped pacing, however, did not interfere with affiliative behavior• In contrast, lesions of orbitofrontal cortex have produced hypoactive animals that show diminished amounts of affiliative as well as agonistic behavior [7,8].
DORSOLATERAL FRONTAL LOBE LESIONS
213
The increased aggression observed in the present experiment had not been seen in field situations where the operate was able to withdraw from contact with other monkeys [6]. In a field setting, a released operate may be confused by the complex array of stimuli that are presented by an awaiting social group. Within this context, he may be unable to separate stimuli and inhibit the response tendency to flee. Withdrawal to a noninteractive, solitary situation results. Perhaps within the confines of the laboratory enclosure, the operated monkey is forced into contact with others and is unable to express the proper signals to avoid direct attack. In the limited space of the enclosure, these displays are necessary to avoid such contacts and, frontal animals, unable to express them, cannot avoid these encounters and aggress more. However, by the same token, affiliative behavior is maintained (Fig. 3) in the present setting. This indicates that frontally lesioned monkeys in a restricted spatial environment can maintain affiliations but, at the same time, change agonistic responses. In a study carried out in a group of stump-tailed macaques sustaining dorsolateral frontal lesions, social
affiliative behavior in an expanded spatial context (1/2 acre) is being compared to behavior of the same group obseryed in a laboratory enclosure. Preliminary results indicate that there is a relative increase in spatial distancing by operates from the core group in the 1/2 acre enclosure. A theoretical model of frontal lobe function incorporating attention and stimulus processing proposed by Konorski and Lawicka helps to account for the inability of the operate to sort out incoming information and resort to aggression in the face of the resultant confusion [3]. We have seen in the operated monkey the ability to maintain affiliative relations with other group members and to interact with them, (e.g. grooming, joining and playing). However, they no longer utilize facial expression and resort to direct aggression. Perhaps because of a perceptualcognitive deficit, the frontal monkey is unable to perceive and/or react to complex stimulus situations nor to inhibit certain responses to these stimuli. In conclusion, a model of frontal lobe damage that suggests difficulty in stimulus processing and failure of inhibitory mechanisms that are exacerbated by the hyperactive state may serve to explain the results of this study.
REFERENCES 1. Brody, E. G. and H. E. Rosvold. Influence of prefrontal lobotomy on social interaction in a monkey group. Psychosom. Med. 14: 406-415, 1952. 2. Deets, A. C., H. F. Harlow, S. D. Singh and A. J. Blomquist. Effects of bilateral lesions of the frontal granular cortex on the social behavior of rhesus monkeys. J. comp. physiol. Psychol. 72: 452-461, 1970. 3. Konorski, J. and W. Lawieka. Analysis of errors by prefrontal animals on the delayed response test. In: The Frontal Granular Cortex and Behavior, edited by J. M. Warren and K. Akert. New York: McGraw-Hill,1964, pp. 271-294. 4. Mass, R. The effects of dorsolateral ~rontal ablations on social behavior of a caged group of eleven stumptail macaques. Doctoral dissertation, Rutgers UniversityGraduate School, Department of Psychology, 1973.
5. Myers, R. E. Neurology of social communication in primates. Proc. of 2nd International Congr. of Primatology at Yerkes Reg. Primate Ctr. Basel: Karger, 1968. 6. Myers, R. E., C. Swett and M. H. Miller. Loss of social group affinity following prefrontal lesoins in free-ranging macaques. Brain Res. 64: 257-269, 1973. 7. Notkin, E. The effects of orbital-frontal lesions on the social behavior of the caged stump-tailed macaque (Macaca speciosa). Master's thesis, Rutgers University Graduate School, Department of Psychology, 1972. 8. Snyder, D. R. Fall from social dominance following orbital frontal ablation in monkeys. Proceedings 78th Annual Convention, APA, 1970.