mise à jour du
13 avril 2008
Displacement Activities
as a Behavioral Measure of Stress
in Nonhuman Primates and Human Subjects
Alfonso Troisi
Department of Psychiatry, University of Rome, Italy


Traditionally, research on human stress has relied mostly on physiological and psychological measures with a relatively minor emphasis on the behavioral aspects of the phenomenon. Such an approach makes it difficult to develop valid animal models of the human stress syndrome. A promising approach to the study of the behavioral correlates of stress is to analyze those behavior patterns that ethologists have named displacement activities and that, in primates, consist mostly of self-directed behaviors. In both nonhuman primates and human subjects, displacement behavior appears in situations characterized by social tension and is likely to reflect increased autonomic arousal. Pharmacological studies of nonhuman primates have shown that the frequency of occurrence of displacement behavior is increased by anxiogenic compounds and decreased by anxiolytic drugs. Ethological studies of healthy persons and psychiatric patients during interviews have found that increased displacement behavior not only correlates with a subjective feeling state of anxiety and negative affect but also gives more veridical information about the subject's emotional state than verbal statements and facial expression. The measurement of displacement activities may be a useful complement to the physiological and psychological studies aimed at analyzing the correlates and consequences of stress.
The phenomenology of the stress syndrome involves three distinct response modalities: physiological reactions, subjective feelings and behavioral changes (Chrousos and Gold, 1992). Traditionally, studies of human subjects have concentrated on the measurement of physiological and subjective correlates of stress. Much less attention has been paid to the description and measurement of the behavioral changes that are elicited by exposure to stressful situations. While this approach has contributed much to our understanding of the stress syndrome, it is not without its limitations. These include the difficulty in comparing human and animal data and reliance on selfreports that are of unknown reliability. Not knowing how a subject feels or what are its psychic experiences restricts the animal researcher to inferences based on observable behaviors. Conversely, assessment of stress in human subjects is based almost exclusively on the evaluation of the psychic experiences as voiced by the subject. Because of this difference between the methods employed in human and animal studies, the integration of human and animal data is generally difficult and sometimes impossible. Another problem is the reliability of subjects' reports of their psychological status. Selfreports may be unreliable not only because of conscious deception or unconscious masking but also due to inaccurate self-evaluation. The complexity of the relationship between subjective and objective aspects of mental distress becomes clear on reading the results of alexithymia studies in this article. A prerequisite for the behavioral study of stress in human subjects is the identification and description of motor patterns that are consistently associated with the stress response and that have a phylogenetic basis. In this regard, a promising approach is the analysis of those behavior patterns that ethologists have named displacement activities and that consist mostly of movements focused on one's own body such as self-touching, scratching and self-grooming. The aim of this article is to review ethological, physiological and pharmacological data suggesting that displacement activities are a valid behavioral measure of stress in nonhuman primates and human subjects.
The ethology and physiology of displacement activities
Ethologists commonly use the term "displacement activity" to designate behavior patterns occurring in situations in which they would not expect to observe them (McFarland, 1966). For example, a male three-spined stickleback (Gasterosteus aculeatus ), in the midst of courting a female, may suddenly swim to his nest and display fanning behavior, i.e. the parental activity that normally serves to ventilate the eggs in the nest. It is hard to explain how such a behavior is relevant to either parental care (as there are still no developing eggs in the nest) or courtship (as the fanning activity does not appear to influence the female). Such "irrelevant" behavior is common during fighting, agonistic contest, courtship and play of all vertebrate animals. It has been commonly referred to as "displacement behavior" because early ethologists thought it was not "fed" from its own sources but by "displaced" energy originating from a different source blocked in its normal expression (Kortmulder, 1998).
Displacement activities are common in situations of motivational conflict in which tendencies to perform more than one activity are simultaneously expressed. For example, the displacement fanning of the male threespined stickleback described above is most likely to occur when there is equilibrium between the conflicting tendencies to attack and to court a female that enters the territory. Displacement activities also appear in situations in which a goal-directed behavior is thwarted by internal or external factors (e.g. frustration). In nonhuman primates, by far the most common displacement activities are those "comfort behaviors" that have something to do with body care such as grooming, scratching, shaking, stretching or yawning. Much less common are feeding, sleeping, sexual mounting, and parental behavior. In human beings, displacement activities include both self-directed behaviors similar to primate grooming behavior (e.g. head scratching, beard stroking) and aimless, iterative manipulation of objects (e.g. sucking on pens, twisting wedding rings, fingering handkerchiefs). Table I lists the behavior patterns included in the category "displacement behavior" of the Ethological Coding System for Interviews (ECSI; Troisi, 1999), an ethogram designed for measuring nonverbal behavior during interviews. The frequency of occurrence of displacement behavior as defined by the ECSI is fairly high, ranging from 20 to 100% of the sample intervals.
Such a wide variation depends on a number of factors, including the content of the interview, the age and sex of the interactants, and the diagnostic status of the interviewee (normal subjects, psychiatric patients with anxiety, depressive, or psychotic disorders). The fact that displacement activities derive from behaviors that, in the appropriate context, fulfil practical functions raises the question of how to make a distinction between these normal behaviors and the corresponding displacement activities. In some cases, there are morphological differences between a displacement activity and the same activity carried out in its normal context. Studying behavioral indicators of anxiety in captive group-living chimpanzees (Pan troglodytes ), Baker and Aureli (1997) found that rough scratching (defined as raking one's own hair or skin with fingernails including large movements of arm), but not gentle scratching (defined as raking one's own hair or skin with fingernails including mainly movements of hand or fingers), increased during periods with high levels of neighbor vocalization (see the section on behavioral studies in nonhuman primates). Russell and Russell (1985) argued that "a displacement activity is always fragmentary and incomplete, when compared with the same activity carried out in its normal mood and context." (p. 31). However, in most cases, displacement behavior can only be defined by its context of occurrence, not by its morphology, and it is often impossible to indicate exactly where a displacement activity merges into original behavior (Kortmulder, 1998). The vagueness of the boundaries between the two categories of behavior is further confirmed by the finding that displacement activities are, to some extent, influenced by the same external stimuli that normally elicit the corresponding original behavior. For example, domestic cocks show bouts of feeding or drinking during fights. If water is available displacement drinking occurs, and if food is available displacement feeding occurs.
Another question that needs to be addressed is the relationship between displacement activities and other behaviors that apparently serve no obvious purpose. Some terms that have been used in the literature are in fact synonymous of displacement activities (i.e. ritualized conflict behavior, vacuum behavior, irrelevant behavior, incongruous behavior, redirected behavior). In contrast, the term "stereotypy" has been used more ambiguously and may indicate motor acts that differ from displacement activities in terms of etiology and physiological mechanisms. Whereas displacement activities are normal behaviors that can be observed in natural settings, "true" stereotypies are pathological behaviors exhibited by individuals subjected to social and sensory isolation (Ridley and Baker, 1982). In nonhuman primates living in captivity, stereotypies can take the form of self-clasping, compulsive masturbation, head tossing, rocking, stereotyped pacing, or bouncing in place (Erwin and Deni, 1979). Similar behaviors have been observed in institutionalized patients suffering from psychotic disorders or mental retardation. These behaviors do not resemble, and should not be confused with, displacement activities. Less clear is the relationship between displacement activities and those repetitive actions fixed in form and orientation that have been observed in farm animals and that have been claimed to reduce tension or anxiety through release of brain opioids (Dantzer, 1986). Although these behaviors have been labeled as "stereotypies", the fact that they are self-directed behaviors typically observed in situations of conflict or frustration suggests a significant overlap with displacement activities. The hypothesis that displacement behavior may result from autonomic processes activated during stressful situations has been repeatedly advanced in the ethological literature. For example, several authors have suggested that, in a variety of species, the mechanism responsible for displacement activities consisting of brief skin-care patterns involves peripheral somatic changes (e.g. increased peripheral blood flow, sweating), which may in turn lead to behavioral responses (e.g. scratching) (Delius, 1967; Hinde, 1982). However, displacement behavior might be directly controlled by central mechanisms as well. In rats, the intracerebroventricular injection of corticotropin-releasing factor (CRF) (Dunn and File, 1987) or adrenocorticotropic hormone (ACTH) (Gispen and Isaacson, 1981) causes a remarkable elevation of grooming, a self-directed behavior commonly observed under stressful conditions. In primates, direct evidence that displacement activities are associated with stress-related physiological changes is lacking, even though circumstantial evidence suggests that this may be the case. Studies of captive macaques have found that both heart rate and frequency of scratching increase following an episode of aggression and both are reduced after the individual is groomed by other monkeys (Schino et al., 1988; Aureli et al., 1989; Boccia et al., 1989).
Nonhuman primate studies
Behavioral Studies Behavioral studies of nonhuman primates living in groups have demonstrated that the occurrence of displacement behavior is associated with a variety of social situations that are apparently quite heterogeneous but which have in common uncertainty and anxiety as the stressful causal factors (Maestripieri et al., 1992b). Uncertainty about assessment of dominance rank is a social situation associated with high levels of displacement activities. Schino et al. (1990) found that, when two unfamiliar female long-tailed macaques (Macaca fascicularis ) were paired in a cage, the delayed establishment of dominance relationships caused a sharp increase in the frequency of scratching and self-grooming. Such an increase did not occur when the pairing involved either unfamiliar monkeys who rapidly displayed behavioral indicators of status differences or familiar individuals with already established dominance relationships. Uncertainty about the risk of being attacked is another situation commonly associated with increased levels of displacement activities. Troisi and Schino (1987) found that the rate of self-grooming in female long-tailed macaques increased when the subjects were in spatial proximity (within 1m) with the dominant male. Adult female macaques are attracted by the dominant male and have the tendency to approach him to groom him or to sit in bodily contact with him. However, spatial proximity with the dominant male is a potentially risky situation because sometimes the male reacts by attacking the approaching female. Baker and Aureli (1997) found that, in captive group-living chimpanzees, the rate of scratching increased after the exposure to vocalizations of neighboring groups, an acoustic signal associated with a high risk of impending intragroup aggression. Displacement activities have also been reported to occur immediately after agonistic interactions. In longtailed macaques and olive baboons (Papio anubis ), intragroup aggression is followed by a dramatic increase in the rate of scratching, in both the victim of aggression (Aureli and van Schaik, 1991; Aureli, 1992; Castles and Whiten, 1998) and the aggressor (Aureli, 1997; Castles and Whiten, 1998). Such an increase reflects the uncertainty of the post-conflict situation. The victim of aggression cannot be sure it will be tolerated around resources by the former aggressor and it is more likely to be attacked again, whereas the aggressor may lose the support of its previous opponent for future cooperative actions (see the review by Aureli and Smucny (2000) for data supporting such an interpretation). Displacement behavior appears to be a sensitive measure of the intensity of the stress experienced in the post-conflict phase. Aureli (1997) found that, in longtailed macaques, scratching rates were higher after unreconciled conflicts between "friends" (i.e. partners with previous high affiliation rates) than after those between other individuals. This finding has two important implications for a better understanding of the link between social stress and displacement behavior. First, stressrelated increase in displacement activities is a response of variable intensity influenced by the specific characteristics of the social context rather than a none-or-all reaction. Second, anxiety elicited by a potential danger for one self's physical integrity or social status is not the only stressful situation correlated with an increase in the rate of displacement activities. Also a perceived danger to either a valuable relationship or a significant other can be the proximate cause of this behavioral response. Data illustrating this latter aspect come from studies of mother&endash;infant pairs.
Studying maternal behavior in captive Japanese macaques (Macaca fuscata ), Troisi et al. (1991) found positive correlations between rates of scratching and maternal possessiveness. Thus, mothers who were most apprehensive about their infants and adopted a highly protective style of mothering were also those who scratched themselves more. In a study of maternal anxiety in rhesus macaques (Macaca mulatta ), Maestripieri (1993) found that the rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants were in spatial proximity to the adult male or higher-ranking adult females. Furthermore, the rate of maternal scratching increased when infants approached or were approached by individuals who frequently harassed them. Pharmacological Studies In nonhuman primates, evidence indicating an association between stress and displacement activities is not limited to behavioral observations. Several studies have employed experimental manipulations to investigate the neurobiological correlates of displacement behavior and its relationships with negative emotional states. Redmond and Huang (1979) demonstrated that the electrical and pharmacological activation of the locus coeruleus, a major brain noradrenergic nucleus which mediates anxiety-related behaviors, elicits scratching in the stump-tailed macaque (Macaca arctoides ). In line with this finding, treatment of chair-restrained rhesus monkeys with the anxiogenic compound beta-CCE has been reported to elicit not only physiological changes typically associated with the stress response but also a variety of behavioral changes including increased scratching (Ninan et al., 1982). Studies conducted in more ecologically-valid settings have confirmed the association between displacement activities and anxiety. Schino et al. (1991) studied the effects of the acute administration of lorazepam, an anxiolytic drug, on scratching by group-living female long-tailed macaques with particular reference to the modulating influence of social rank. Lorazepam reduced scratching in both high-ranking and low-ranking subjects but the effect was more marked in low-ranking females. The authors explained this finding arguing that especially low-ranking animals are prone to experience stressful social situations. In effect, they found that baseline scratching was higher in low-ranking than in high-ranking monkeys. Maestripieri et al. (1992a) investigated the effects of anxiolytic and anxiogenic treatments on the behavior of rhesus monkey infants living with their mothers and other group companions. These authors found that the anxiogenic beta-CCE increased the frequency of both infant scratching and contact-seeking behavior with the mother. In contrast, the acute administration of the anxiolytic midazolam reduced the rate of infant scratching.
Schino et al. (1996) investigated the acute effects of two benzodiazepine receptor ligands with opposite effects (i.e. the anxiolytic lorazepam and the anxiogenic FG 7142) on the displacement activities of seven male long-tailed macaques living in social groups. In line with the hypothesis of the study, lorazepam caused a dosedependent decrease in the frequency of displacement activities, whereas the beta-carboline FG 7142 caused a dose-dependent increase (Fig. 1). Drug effects on other behaviors that could alter the emotional state of the animal or the cutaneous stimuli eliciting displacement activities did not mediate these changes. The most interesting finding of this study was that displacement activities were apparently more sensitive to anxiolytic treatment than other behavior patterns indicative of an anxiety state. The non-sedative low doses of lorazepam that were used did not affect either visual scanning of the social environment nor fear responses directed to dominant males, two behavior patterns that reflect anxiety as demonstrated by their increase after treatment with FG 7142. Nevertheless, the same doses of lorazepam were sufficient for decreasing the frequency of displacement activities.
Human studies
In the literature on human nonverbal communication, displacement activities have been referred to by many labels, including synkinetic movements (Allport and Vernon, 1933), autistic movements (Krout, 1935), self-manipulations (Rosenfeld, 1966a), body-focused movements (Freedman and Hoffman, 1967), self-adaptors (Ekman and Friesen, 1969), and body manipulators (Ekman, 1977). Even though the interest in these behavior patterns dates back to the 1930s, the evidence linking stress with self-directed behavior in human subjects is relatively limited when compared to the extensive literature on nonhuman primates. Self-contact actions were found to increase in response to experimentally induced withdrawal of socially supportive nonverbal behavior (Rosenfeld, 1967), and their rate of occurrence was found to correlate with ratings of anxiety and guilt (Ekman and Friesen, 1972), as well as disapproval (Rosenfeld, 1966b). Waxer (1977) found that raters naive to the content of a clinical interaction were able to identify the presence of anxiety and its intensity on the basis of nonverbal cues alone. Examining silent video segments drawn from interviews with psychiatric patients, raters perceived nonillustrative hand movements (e.g. stroking oneself) as the most salient cues to anxiety and were able to distinguish between patients with high and low scores on a self-rating scale for anxiety. Shreve et al. (1988) analyzed the nonverbal behavior of 25 patients during their interactions with family practitioners. Patient interviews were categorized on the basis of topic content into two types: dual-agenda interviews and single-agenda interviews. Dual-agenda interviews contained two conditions: an initial topic (i.e. first agenda) judged not to be the most significant complaint expressed by the patient, and a later presentation of a psychosocial need that was emotionally relevant to the patient (i.e. hidden agenda). Single-agenda interviews contained only a single topic presented by the patient. Hand-to-body self-touching occurred significantly more often during patient presentation of conflicted emotional topics (i.e. hidden agendas), while frequencies of speech-illustrative gestures did not differ for type of agenda presented. Troisi et al. (1998) used the Ethological Coding System for Interviews (ECSI) to analyze the nonverbal behavior of 28 young men with a diagnosis of recent-onset schizophrenia.
Most of these patients had never received neuroleptic treatment and all of them were kept drug-free for at least a week prior to being interviewed. At the end of the interview, the clinician rated patients' symptoms on the Brief Psychiatric Rating Scale (BPRS), a psychometric instrument that covers the entire range of schizophrenic psychopathology. There was a positive and significant correlation between displacement behavior and the anxiety/depression subscale of the BPRS. Those patients who were rated as most anxious and/or depressed by the clinician showed a higher frequency of displacement activities during the interview (Fig. 2). Taken together, the results of these studies indicate that, in human subjects, displacement activities may be elicited by stressful stimuli and may reflect an emotional condition of negative affect (i.e. anxiety and/or depression). However, the relationship between stress-related emotional state and displacement activities may be more complex than that emerging from the findings reported above, as suggested by two recent studies of nonverbal behavior correlates of alexithymia (Troisi, et al., 1996; 2000. Alexithymia is a personality trait distributed normally in the general population which involves a marked difficulty in identifying feelings and describing them to other people (Bagby and Taylor, 1997). Alexithymic individuals know very little about their own feelings and, in most instances, are unable to link negative affect with memories, fantasies, or specific situations. The alexithymia construct is relevant to stress research because a deficit in modulating distressing emotions through cognitive processing might result in exacerbated responses in the autonomic nervous system. Several psychophysiological studies have yielded preliminary evidence that alexithymic individuals show higher tonic levels of sympathetic arousal than nonalexithymic individuals (Friedlander et al., 1997; Infrasca, 1997), and a decoupling of the autonomic and cognitive responses to laboratory stressors (Papciak et al., 1985; Martin and Pihl, 1986; Rabavilas, 1987). In addition, there is evidence that alexithymia is associated with a variety of psychiatric and medical disorders (Taylor, 2000). Using the ECSI, Troisi, et al., 1996 studied the relationship between alexithymia and nonverbal behavior in 24 young volunteers free of medical and psychiatric disorders. Multiple regression analysis controlling for the levels of anxiety and depression revealed that the frequency of self-directed behavior during the interview was a significant predictor of alexithymic traits. Those subjects who had more difficulty identifying and describing their feelings scored higher on the category of the ECSI measuring displacement activities. Similar findings have emerged from a more recent study conducted on 30 patients with depressive or anxiety disorders (Troisi et al., 2000). The patients with more pronounced alexithymic features showed a significantly higher frequency of displacement activities during interviews.
At the same time, these patients reported levels of self-rated anxiety and depression equivalent to those reported by nonalexithymic patients. These findings have two important implications for studies of the relationship between stress and displacement activities. First, one should not expect to find the occurrence of displacement behavior invariably associated with self-reports of negative affect. Some individuals have a reduced ability to experience and regulate affects cognitively, and this can produce an apparent dissociation between subjective appraisal of emotion and nonverbal behavior reflecting increased emotional arousal. Second, in stress research, the recording of displacement activities may be a useful complement to psychological assessment because nonverbal behavior can give more veridical information about the subject's emotional state than verbal statements. This concept was originally expressed by Ekman and Friesen (1969) who coined the term "emotional leakage". These authors argued that the behavior patterns that they labeled as selfadaptors (largely corresponding to the displacement activities listed in the ECSI) "leak more," that is, they reflect the subject's affective state more accurately than self-reports on emotion which are often subject to either greater conscious deception or unconscious masking.
Symptoms or adaptive responses?
Most of the physiological changes occurring during acute stressful situations are adaptive responses that attempt to counteract the effects of the stressors in order to reestablish homeostasis (Chrousos and Gold, 1992). Could we say the same for displacement behavior? Are displacement activities behavioral components of the adaptive stress response? Studies of non-primate species suggest that this is the case. Behavioral "stereotypies" attenuate physiological measures of stress (Dantzer and Morme`de, 1985) and stimulate endorphin production (Cronin et al., 1986) in pigs. Displacement chewing and gnawing reduce the stress-related activation of the hypothalamo-pituitary&endash; adrenal axis in mice exposed to novel environment (Hennessy and Foy, 1987) and in rats exposed to electric shock (Levine et al., 1989). In rats and mice exposed to a brightly lit novel environment, animals that engaged in displacement chewing of inedible objects displayed significantly lower activation of the prefrontal cortical dopaminergic system, which is generally observed in stressful situations (Berridge et al., 1999). Since the attenuation of the stressor-induced increase in dopaminergic transmission within the prefrontal cortex is similar to that observed following administration of anxiolytics and opposite to that observed following administration of anxiogenics, Berridge et al. (1999) have suggested that displacement chewing may serve an anxiolytic function. In primates, very few studies have tested the hypothesis that displacement activities may be adaptive responses evolved to cope with stress. In a prosimian species, the small-eared bushbaby (Otolemur garnettii ), the animals that performed more displacement activities (foot and chest rubbing) in a novel environment also exhibited lower cortisol responses to restraint stress (Watson et al., 1999). Among olive baboons living freely in a national park in Africa, those subordinate males that were most likely to displace aggression onto a third party after losing a fight had significantly lower basal glucocorticoid concentrations compared to the remaining subordinate cohort (Virgin and Sapolsky, 1997). However, the relevance of this finding to the stress-reducing function of displacement activities is dubious. Even though fighting has been included among primate displacement activities (Russell and Russell, 1985), redirected aggression might be a physiological and behavioral phenomenon completely different from self-directed behaviors such as scratching or self-grooming. In humans, the evidence is, at best, circumstantial and limited to the finding that gentle body touching causes relaxation and a reduction in heart rate (Drescher et al., 1980). Several considerations concur in suggesting that displacement activities are behavioral components of the adaptive stress response, probably causing anxiolytic effects. They are widespread across the phylogenetic scale, their frequency of occurrence is fairly high in both natural and experimental settings, and individuals free from behavioral pathologies exhibit them. Nevertheless, definitive evidence for a physiological and/or behavioral function of displacement activities performed by nonhuman primates and humans under stress is still lacking.
The data reviewed in this article suggest that displacement behavior is a valid measure of stress in nonhuman primates and human subjects. The measurement of displacement activities can be introduced into studies aimed at analyzing the behavioral correlates of human stress as a useful complement to physiological and psychometric assessments. Clearly, the use of displacement activities as a behavioral measure of stress requires a greater investment of time and resources than is needed for most of the procedures currently employed in psychophysiological research. Direct observation and quantitative recording of behavior are time-consuming and much more complicated than psychometric assessment. However, what is lost in The fact that there are already sufficient data to justify the use of displacement activities in human stress research does not mean that we have a complete knowledge about the causation and function of these behavior patterns. Many questions remain to be answered. What are the physiological mechanisms implicated in the proximate causation of displacement behavior? Do displacement activities serve an adaptive role in reducing autonomic activation? Are different types of displacement activities equivalent in terms of validity for measuring stress? To answer these and other questions, further research on human displacement behavior should be based on studies that integrate ethological observation, physiological measures, and psychometric assessment. The correspondence between physiological changes and variations in the frequency of occurrence of displacement activities should be measured in subjects exposed to different levels of experimental social stress. Concurrent psychometric assessment should clarify whether or not self-reported levels of anxiety co-vary with the behavioral and physiological measures. The short- and long-term effects of displacement activities on the physiological parameters implicated in the stress response should be evaluated. If an anxiolytic effect of displacement activities were demonstrated, investigators should ascertain whether different motor patterns included in the category of displacement behavior (e.g. scratching vs. gentle and prolonged selfcontact) differ in terms of efficacy in calming down the subject under stress.
TABLE I Definition of behavior patterns included in the category "displacement behavior" of the Ethological Coding System for Interviews (ECSI)
1. Groom. The fingers are passed through the hair in a combing movement.
2. Hand&endash;face. Hand(s) in contact with the face.
3. Hand&endash;mouth. Hand(s) in contact with the mouth.
4. Scratch. The fingernails are used to scratch part of the body, frequently the head.
5. Yawn. The mouth opens widely, roundly and fairly slowly, closing more swiftly. Mouth movement is accompanied by a deep breath
and often closing of the eyes and lowering of the brows.
6. Fumble. Twisting and fiddling finger movements, with wedding ring, handkerchief, other hand, etc.
7. Twist mouth. The lips are closed, pushed forward and twisted to one side.
8. Lick lips. The tongue is passed over the lips.
9. Bite lips. One lip, usually the lower, is drawn into the mouth and held between the teeth.
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