mise à jour du
20 avril 2006
Am J Primatol
2004; 63; 2; 41-48
Extinction deficits in male rhesus macaques with a history of self-injurious behavior
Lutz C, Tiefenbacher S, Meyer J, Novak M.
New England Primate Research Center, Southborough, Massachusetts, USA.


Self-injurious behavior (SIB) occurs in both human and nonhuman primate populations. Despite the potential for harm, SIB may persist in part because of an inability to inhibit behavior that results in wounding. A lever-pressing task was used to test the prediction that monkeys with SIB would show greater persistence in lever-pressing on extinction trials than monkeys without the disorder.
The subjects were 15 individually-housed adult male rhesus macaques, 10 of which (the SIB group) had a veterinary record of self-inflicted wounding. All of the monkeys were trained to lever-press for food rewards to a criterion of 400 total responses. The test procedures consisted of five daily 30-min sessions divided into six 5-min intervals. On day 1, the subjects received continuous reinforcement. On days 2-4, testing consisted of alternating reinforced/unreinforced 5-min intervals, beginning with reinforcement. Reinforced intervals were cued with a buzzer. On day 5, the subjects received no reinforcement. The number of lever-presses and behavioral responses were recorded during each session. Saliva samples were collected for cortisol measurement before and after test sessions on days 1, 2, and 5.
As predicted, monkeys with SIB lever-pressed more than controls during extinction intervals on days 2-4. There was no difference on day 1 or day 5. The frequency of scratching, yawning, and abnormal behavior increased when reinforcement was intermittent (days 2-4) or absent (day 5). Cortisol levels were highest with continuous reinforcement (day 1), and may reflect differential levels of food intake rather than stress. The presence of extinction deficits suggests that SIB may persist in some monkeys because they lack the ability to regulate the intensity of their biting behavior.
Self-injurious behavior (SIB) is a potentially destructive behavior that occurs in both human and nonhuman primate populations. SIB in humans often takes the form of self-cutting, self-biting, and head-banging, without suicidal intent [Carr, 1977; Favazza & Rosenthal, 19931. The rate of SIB tends to be higher in subjects with mental retardation (10.-14%) [Griffin et at, 1986; Maisto et al., 1978; Schroeder et al., 1978] than in the general population (4%) [Briere & Gil, 1998; Klonsky et al., 2003]. However, individuals with genetic disorders, such as Lesch-Nyhan or Rett syndromes, are also known to commit self-mutilating acts [Anderson et al., 1978; Coleman et al., 1988; Nyhan, 1976]. Environmental risk factors associated with SIB include restrictive housing conditions, such as institutional rearing of children IjBeckett et al., 2002] and adult internment in correctional facilities [Boiko & Lester, 2000].
Similarly to humans, some macaque monkeys may also develop an SIB syndrome [Bayne et al., 1995; Bellanca & Crockett, 20021, which can take the form of head-banging, excessive hair-pulling, and self-directed biting, occasionally resulting in self-inflicted wounding [Bayne & Novak, 1998; Novak, 2003]. Risk factors for SIB in these animals include variables such as individual housing at an early age or for an extended period of time tiBellanca & Crockett, 2002; Lutz et al., 2003a]. Although environmental factors may predispose an animal to develop SIB, specific triggers or experiences may be needed to initiate the actual selfinjurious act. For example, stressful situations such as being moved to a novel room [Lutz et al., 2003b) or subjected to repeated blood draws [Lutz et al., 2003a] have been associated with an increase in self-directed biting or wounding. With repetition of stressful triggers, SIB may become ritualized, i.e., less variable, more automatic, and more easily activated [Dantzer, 1986].
Even though SIB may cause pain and/or injury, it persists in captive populations of macaque monkeys. Recent surveys of individually-housed macaques found that approximately 25% of the animals exhibited self-biting behavior [Lutz et al., 2003a]. However, a smaller portion of this population (5-11%) produced wounds that required veterinary care [Bayne et al., 1995; Bellanca & Crockett 2002; Lutz et al., 2003a1.
It is unclear why some animals bite themselves without wounding, while others bite and wound. One possible explanation is that wounders find it more difficult to inhibit their injurious behavior than other monkeys. Lending some credence to this view is an early study by Gluck and Sackett [19761, in which a lever-pressing task was used to assess extinction deficits (i.e., continuing to leverpress in the absence of rewards) in monkeys reared in isolation. Isolation rearing is a major predictor of SIB in rhesus monkeys, and the isolate-reared monkeys took longer than the controls to extinguish their lever-pressing behavior. In the present study, we used a lever-pressing procedure to examine the relationship between SIB and extinction deficits in socially reared monkeys. Thus, SIB in this population was not the result of impoverished early rearing. If SIB is a manifestation of an inability to inhibit certain kinds of behavior, then it should take monkeys with an SIB syndrome longer to extinguish their lever-pressing behavior compared to monkeys with no wounding history.
Monkeys with a veterinary record of self-inflicted wounding showed more persistence in lever-pressing during extinction intervals on days 2-4 than those without such a record. This result suggests that monkeys with a history of SIB may be unable to inhibit the behaviors that lead to wounding. At the present time, it is unclear whether the problem is one of suppressing biting behavior or of regulating the intensity of the biting response. The latter view is supported by the fact that some monkeys habitually bite themselves but do not wound themselves.
Differences in response to extinction cannot be explained by differences in motivation between monkeys with and without SIB. The groups did not differ in the number of training sessions required to meet the criterion, and there were no group differences in lever-pressing when the monkeys were exposed to Continuous Reinforcement (day 1 of testing). Both groups also showed a rapid cessation of lever-pressing when exposed to the No Reinforcement condition (day 5 of testing). This latter point is interesting because it suggests that the extinction deficit was present only when reward alternated with nonreward, and did not carry over from the intermittent condition (days 2-4) to the nonrewarded condition on day 5.
All of the monkeys responded somewhat negatively to the changing reinforcement contingencies. Abnormal behavior, scratching, and yawning increased when reinforcement was intermittent (days 2-4) or absent (day 5). Thus, exposure to extinction appeared to produce some behavioral tension, regardless of group. However, the cortisol results did not parallel the behavioral reactions: the condition that elicited the fewest behavioral responses (Continuous Reinforcement) resulted in the highest level of cortisol. Food consumption has been shown to increase cortisol levels in humans tHansen et al., 1997; Korbonits et al., 1996; Rosmond et al., 2000]. In the present study, both food intake and salivary cortisol levels were greatest on day 1, which suggests that the difference in cortisol across days may be due more to food intake than to stress.
Taken together, these data suggest that monkeys with SIB may have difficulty regulating or controlling their responses under certain conditions. The presence of extinction deficits in some captive macaques may help to explain why some animals persist in biting to the point of injury.

Self-injurious behavior in male rhesus macaques does not reflect externally directed aggression.
Physiol Behav. 2003;78(1):33-39.
Lutz C, Marinus L, Chase W, Meyer J, Novak M.
Self-injurious behaviors (SIB), such as self-biting and self-wounding, have been observed in a small percentage of captive nonhuman primates. Because rhesus monkeys that exhibit SIB also tend to be more aggressive, it was hypothesized that SIB is related to externally directed aggression and is associated with contexts in which physical contact between participants is prevented. The purpose of this study was to test the hypothesized relationship between SIB and outward aggression. Subjects were first presented with videotapes of conspecifics, scenery and a blank screen, and their behavior was recorded. Levels of salivary cortisol, an indicator of stress, were also measured before and after presentation of the videos. Although aggression increased when subjects viewed tapes containing conspecifics, neither cortisol levels nor self-biting behavior varied as a function of tape content. The subjects were then placed in two additional test situations: an empty room and the same room containing an unfamiliar conspecific. Aggression was significantly higher in the stranger condition compared to the empty room condition. The two situations yielded parallel increases in cortisol, suggesting that being alone was just as stressful as being paired with an unfamiliar conspecific. Self-biting rates were also similar in these two conditions. Thus, contrary to our prediction, increases in aggression did not correlate with increases in SIB. These results suggest that under similarly stressful conditions, SIB and externally directed aggression are unrelated.

Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience.
Am J Primatol. 2003;60(1):1-15.
Lutz C, Well A, Novak M.
Abnormal behavior in captive rhesus monkeys can range from active whole-body and self-directed stereotypies to self-injurious behavior (SIB). Although abnormal behaviors are common in singly-housed rhesus monkeys, the type and frequency of these behaviors are highly variable across individual animals, and the factors influencing them are equally varied. The purpose of this investigation was to survey abnormal behavior in a large population of rhesus macaques, to characterize the relationship between stereotypies and self-injury, and to identify potential risk factors for these aberrant behaviors. Behavioral assessments of 362 individually housed rhesus monkeys were collected at the New England Regional Primate Research Center (NERPRC) and combined with colony records. Of the 362 animals surveyed, 321 exhibited at least one abnormal behavior (mean: 2.3, range: 1-8). The most common behavior was pacing. Sex differences were apparent, with males showing more abnormal behavior than females. SIB was also associated with stereotypies. Animals with a veterinary record of self-injury exhibited a greater number of self-directed stereotypies than those that did not self-injure. Housing and protocol conditions, such as individual housing at an early age, longer time housed individually, greater number of blood draws, and nursery rearing, were shown to be risk factors for abnormal behavior. Thus, many factors may influence the development and maintenance of abnormal behavior in captive primates. Some of these factors are intrinsic to the individual (e.g., sex effects), whereas others are related to colony management practices, rearing conditions, and research protocols.

The physiology and neurochemistry of self-injurious behavior: a nonhuman primate model.
Front Biosci. 2005;10:1-11.
Tiefenbacher S, Novak MA, Lutz CK, Meyer JS.
Self-injurious behavior (SIB) is a serious behavioral condition that afflicts millions of individuals in the United States alone. The underlying factors contributing to the development of self-injury in people are poorly understood, and existing treatment strategies for this condition are limited. A low but persistent percentage of socially reared individually housed rhesus monkeys also spontaneously develop SIB. Data obtained from colony records suggest that the risk of developing SIB in socially reared rhesus monkeys is heightened by adverse early experience and subsequent stress exposure. The present review summarizes the physiological and neurochemical findings obtained in this nonhuman primate model of SIB, focusing on monoamine neurotransmitters, neuropeptides, and neuroendocrine systems. The results indicate that monkeys with SIB exhibit long-lasting disturbances in central and peripheral opioid and stress response systems, which lead to increased levels of anxiety. Based on these findings, we propose an integrated developmental-neurochemical hypothesis in which SIB arises from adverse life events in a subset of vulnerable monkeys, is maintained by a persisting dysregulation of several neurochemical and physiological systems, and functions to periodically reduce anxiety when the levels of anxiety become excessive. Implications of this hypothesis for understanding self-injury in patients with borderline personality disorder and members of the general population are discussed.

Tous les travaux de B. Deputte
Tinbergen N Quart Rev Biol 1952;27:1-32
An interpretation of the "displacement phenomenon"
Bindra D British J Psychology 1959:32:236-268
Displacement activities and arousal
Delius J Nature-1967;214:1259-1260
Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects
Troisi A Stress 2002;5(1):47-54
A modest proposal: displacement activities as an indicator of emotions in primates
Maestripieri D, Schino G, Aureli F, Troisi P Anim Behav 1992;44:967-979
The effects of fluoxetine and buspirone on self-injurious and stereotypic behavior in adult male rhesus macaques
Fontenot MB, Padgett EE et al Comp Med 2005;55(1):67-74
Effects of outdoor housing on self-Injurious and stereotypic behavior in adult Male Rhesus Macaques (Macaca mulatta)
Fontenot MB, Wilkes MN, Lynch CS J Am Ass Laboratory Animal Science 2006; 45(5):35-43
Extinction deficits in male rhesus macaques with a history of self-injurious behavior
Lutz C, Tiefenbacher S, Meyer J, Novak M. Am J Primatol 2004;63(2):41-48
Inhibition of social behavior in chimpanzees under high-density conditions
Aureli F, de Waal FB Am J Primatol 1997;41(3):213-28
Frequencies and contexts of gape yawn displays of free-ranging Patas Monkeys
Zucker EL, Gerald MS, Kaplan JR Am J Primatol 1998;45(2):215
Pandiculation: the comparative phenomenon of systematic stretching
Fraser AF Appl Anim Behav Sci 1989;23:263-268
 An ethological interpretation of stereotypy induced by environmental stimulus
Beckmann H, Zimmer R Arch Psychiatr Nervenkr 1981;230(1):81-89
Revue sur le comportement de bâillement chez les vertébrés.
Deputte BL Bull interne société française pour l'étude du comportement animal.1974;1:26-35.
Uber das Gähnen bei Vögeln
Bergmann H Die Vögelwelt 1966;87(5):134-138
Zur Frage des Gähnens bei der Vögel
Löhrl H Die Vögelwelt 1967;88(3):85-86
Maintenance activities
Dilger W Zeitsch. Tierpsychologie 1960;17:649-685
Yawning in the Greenfinch
Harrison JO AUK 1968;55:511
Yawning and other maintenance activities in the South African Ostrich
Sauer EG, Sauer EM The Auk 1967;84:571-587
Zum geruchlichen Beutefinden und Gähnen der Kreuzkröte
Heuser H Zeitschrift für TierPsychologie 1958;15:94-98
New evidence for a locus coeruleus norepinephrine connection with anxiety.
Redmond DE, Wang Y Life Sciences 1979;25(26):2149-2162
Limbic-midbrain lesions and acth-induced excessive grooming
Colbern D et al. Life Sciences. 1977;21:393-402
Aggression does not increase friendly contacts among bystanders in geladas (Theropithecus gelada) Leone A, Mignini M, Mancini G, Palagi E. Primates. 2010;51(4):299-305.