Social interaction over time, implications for stress responsiveness

Social interaction over time, implications for stress responsiveness

Summers, Cliff H

Social Interaction Over Time, Implications for Stress Responsiveness1

SYNOPSIS. Behavioral interaction during social situations is a continuum of action, response, and reaction. The temporal nature of social interaction creates a series of stressful situations, such as aggression, displacement from resources, and the variable psychological challenge of adapting to dynamic social hierarchies. The ebb and flow of neurochemical and endocrine secretions during social stress provide a unique tool for understanding individualized responses to stress. Each social station is an adaptive response to a stressful social condition, resulting in unique neuroendocrine and behavioral responses. By examining the temporal changes of limbic monoamines and plasma glucocorticoids, aspects of mechanisms for adaptation emerge. The similarity of temporal patterns induced by social stress among fish, reptiles and primates are remarkable. Even different specific coping mechanisms point out the similarity of vertebrate stress responses. The lizard Anolis carolinensis exhibits a unique sign stimulus generated during social stress by the sympathetic nervous system that serves as a temporal landmark to distinguish neuroendocrine patterns. During social interaction dominant males have a shorter latency to eyespot darkening than opponents, inhibiting aggressive display. Eyespot coloration can be delayed using a serotonin reuptake inhibitor, causing dominant social status in many animals to be lost. Reversal of social status via serotonergic activation appears to mimic chronic serotonergic activity. The pattern of eyespot darkening, faster in dominant males, is coincident with that for serotonergic activity. The fundamental temporal relationship between dominant and subordinate limbic monoaminergic activity over a continuous course of social interaction appears to be a two-phase response, temporally specific to brain region, and always faster in dominant individuals.


Anyone reading this has experienced social stress of one type or another. Human social stresses are very complex, excessively imbued with emotional content, and like those of other animals, are quite dynamic temporally. Expression of behavior and physiology stimulated by stressful social interaction is the result of mechanisms common to most vertebrate groups, which are temporally resolved. The mechanisms that mediate the common patterns are not yet completely known, but evolutionarily conserved contributions from the hypothalamo-pituitary-adrenocortial (HPA) axis (Selye, 1936; Herbert et al., 1986; Barton and Vijayan, 2002; Wingfield and Kitaysky, 2002), central glucocorticoid receptors (Moore, 2000; Orchinik et al., 2000; Carruth et al., 2002), central activity of HPA– related neuropeptides such as CRF (Bale et al., 2002; Glennemeier and Denver, 2002), the autonomic sympathetic and adrenomedullary secretions (Matt et al., 1997; Korzan et al., 2000a, 2002), and limbic and brainstem monoaminergic systems have been widely reported (Yodyingyuad et al., 1985; Winberg and Nilsson, 1993a; Summers and Greenberg, 1995; Winberg et al., 1997b; Summers et al., 1998). Even invertebrate taxa have stress responses similar to those discovered among vertebrate groups (Stefano et al., 2002), and may employ similar machinery to produce temporally resolved behavioral modification, such as serotonergic activity in lobsters (Huber et al., 2001). Common mechanisms and patterns of expression need not necessarily yield uniform responses, but are potential substrates for evolutionary modification, and the creation of context and species specific stress responses. Within species, variation may result from contextual differences related to morphological type (Knapp and Moore, 1995), seasonal relationship to breeding (Moore, 1987; Kotrschal et al., 1998; Romero et al., 1998; Woodley et al., 2000), weather (Breuner and Hahn, 2000; Romero et al., 2000; Wingfield and Kitaysky, 2002), migration (Romero et al., 1997), captivity (Romero and Wingfield, 1999), and interactions with other neuroendocrine systems, such as testosterone from the gonadal axis (Sapolsky, 1985; Moore et al., 1991; Knapp and Moore, 1997). Groups expressing these neuroendocrine stress response characteristics span a broad spectrum of evolutionary adaptation, and are illustrative of conservation of, and at the same time, specialization of response. Most of all, generalizable neuroendocrine response patterns, attuned by individualized stress responsiveness, are adaptive. They produce context specific behavior, a result of specialized timing for species and even individuals.


Most studies of behavioral and/or neuroendocrine stress responsiveness during aggressive social interaction have emphasized the dramatic effects measured in low-ranking or subordinate males, especially following chronic social interaction (Yodyingyuad et al., 1985; Blanchard et al., 1993; Fuchs et al., 1995; Summers and Greenberg, 1995; Winberg and Lepage, 1998). In contrast, a few investigators have suggested that primarily the dominant animal is significantly stressed, especially under natural conditions, because dominant animals must establish and continually defend territories or maintain priority access to scarce resources (Packer et al., 1995; Creel et al., 1996; Kotrschal et al., 1998). Taken in the appropriate temporal perspective, it is clear that the stress response of one individual influences that of the other (Korzan et al., 2000a, 2002, Fig. 1). Social interaction is a potent stressor, and males exposed to persistent subordination have been demonstrated to have chronically elevated glucocorticoid concentrations (Yodyingyuad et al., 1985; Blanchard et al., 1993; Hoglund et al., 2000; Overli et al., 1999; Winberg and Lepage, 1998) and chronically elevated serotonergic activity (Summers and Greenberg, 1995; Summers et al., 1998), but they also have a fairly fast response to the social stressor. Within 10 min after beginning aggressive social interaction, subordinate male Anolis carolinensis have elevated serotonergic activity (Korzan et al., 2000b, 2001; Summers et al., 2002), elevated plasma catecholamines (Korzan et al., 2000a, 2002) and elevated plasma corticosterone concentrations (Summers et al., 2002). Male A. carolinensis that acquire dominance during an aggressive social contest also have rapidly activated serotonergic, sympathetic and HPA systems (Fig. 2). Similarly in fish, dominant individuals have increased serotonergic activity and elevated cortisol levels early during formation of a dominance hierarchy (Overli et al., 1999). By one day, both dominant and subordinate Arctic chart have elevated brainstem 5-HT synthesis (estimated by precursor tryptophan levels) and use (measured by elevated catabolite 5-hydroxyindoleacetic acid (5-HIAA) concentrations; Winberg and Nilsson, 1993b). In the bicolor damselfish (Pomacentrus partitus), both dominant and subordinate males exhibit a positive correlation between aggression and serotonergic activity, but the activity was expressed in different regions of the brain (Winberg et al., 1996). In dominant males serotonergic activity in hypothalamus is positively correlated with aggressive acts performed. In subordinate males telencephalic 5-HIAA/5– HT is positively correlated with aggression received. Therefore, social interaction is an efficient and physiologically pervasive stressor, rapidly manifest by numerous neural and endocrine systems in both dominant and subordinate males. Similar early neuroendocrine responses from dominant and subordinate animals does not signify that neuroendocrine or behavioral responses remain similar over time.


In both fish and lizards, the stress response resulting from social interactions does not produce any behavioral inhibition in dominant individuals, they remain active and aggressive (Larson and Summers, 2001; Overli et al., 1999). However, male A. carolinensis that become subordinate do begin to show inhibition of aggressive display and attack, developing over time (Fig. 1). The initial aggressive reaction in both dominant and subordinate males is rapid (Two-way repeated measures ANOVA reveal significant time effects, F = 4.993, P 0.1001). These data suggest two things. The first is that both males are actively pursuing social dominance, and it is not genetically obvious who the winner will be. Second, males becoming dominant have the neuroendocrine machinery to respond more quickly to social stress. This is visually verified, for the combatants and observers, by darkening of postorbital skin. Eyespots turn black as early as 5 sec in dominant males (Fig. 1). The average time for eyespot darkening in dominant males is 90 sec; but is delayed in subordinate males until 250 (Larson and Summers, 2001) to 300 sec (Summers and Greenberg, 1994). At the same time subordinate males exhibit eyespot darkening on average, four to five minutes into the fight, overall body color of the subordinate male becomes more brown (Korzan et al., 2002). Dominant males remain green (Greenberg, 1977, 2002). Furthermore, at five minutes there appears to be a reassessment of the dynamics of the interaction, because there is a significant dip (Duncan’s multiple range comparisons, P

Like Anolis, some fish species are also chronically darkened under prolonged social subordination (Hoglund et al., 2000). Behavioral and chromatic differences between dominant and subordinate males overlie differences in neural and endocrine homeostasis (Greenberg, 2002; Fig. 1). In certain extreme cases, where there is no avenue for escape, male A. carolinensis may die from social stress within 24 hr, however many pairs coexist for a month or more. Among males paired for one month, about half the subordinate animals died, even though cover was provided to allow them to avoid social interaction (Summers and Greenberg, 1994). Anoles have a socially and physiologically plastic mechanism for limiting social aggression, darkening of the postorbital skin, or eyespots (Korzan et al., 2000a, b, 2001, 2002). Eyespots act as a sign stimulus to inhibit aggressive display, and appear faster in dominant males. However, if chronic 5-HT is applied pharmacologically to dominant males by the reuptake inhibitor sertraline, eyespot latency is delayed (Fig. 1) and many dominant males become subordinate males (Larson and Summers, 2001). Chronic 5-HT availability may lead to persistent HPA secretions, as 5-HT contributes to ACTH and corticosterone secretion (Abe and Hiroshige, 1974; Winberg et al., 1997a). One of the possible factors contributing to the demise of this subset of persistently subordinate animals is chronically elevated glucocorticoids (Greenberg et al., 1984b).


Although a rapid social activation of the HPA axis produces elevated plasma cortisol concentrations in dominant fish (Overli et al., 1999), following prolonged social interaction in secure social hierarchies, cortisol levels in dominant fish are usually low (Hoglund et al., 2000; Overli et al., 1999; Winberg and Lepage, 1998). This is in contrast with chronically high plasma cortisol in subordinate fish (Elofsson et al., 2000; Hoglund et al., 2000; Overli et al., 1999; Winberg and Lepage, 1998). In A. carolinensis, the patterns of corticosterone secretion also appears to be different for acute and chronic social stress (Fig. 2). Although in both dominant and subordinate males plasma corticosterone is elevated early (by 10 min) during social stress and diminishes by 20 min, thereafter only subordinate males have re-elevated plasma corticosterone (Greenberg et al., 1984b; Summers et al., 2002). After three weeks cohabitation and presumably some social stress, corticosterone concentrations appear to have remained chronically elevated in subordinate, but not dominant, males (Greenberg et al., 1984b). Subordinate fish (Winberg and Lepage, 1998) and subordinate monkeys (Yodyingyuad et al., 1985) also have chronically elevated glucocorticoid levels, measured at from a week to a month of social interaction. Hormonal responses to stress have been demonstrated to vary dependent on social status in many types of vertebrates, encompassing fishes (Winberg and Lepage, 1998; Elofsson et al., 2000), reptiles (Summers et al., 2002), birds (Kotrschal et al., 1998; Wingfield and Kitaysky, 2002) and mammals (Blanchard et al., 1993; McKittrick et al., 1995) including primates (Sapolsky, 1983; Yodyingyuad et al., 1985). Temporal resolution of the glucocorticoid response suggests a dynamic secretory pattern for corticosterone due to social stress in A. carolinensis, with acute elevation common to both dominant and subordinate males (Fig. 2), and chronic elevation measured in subordinate animals (Summers et al., 2002).


Peripheral responses, especially corticosterone or cortisol, to social stress and aggression are the most widely chosen measures of stress responsiveness (Christian, 1963, 1968; Sapolsky, 1983; Winberg and Lepage, 1998; Brenner and Hahn, 2000; Barton and Vijayan, 2002; Carruth et al., 2002; Wingfield and Kitaysky, 2002). Although most investigators report a fairly rapid and robust glucocorticoid response to stress (Moore et al., 1991; Moore, 2000; Orchinik et al., 2000; Woodley et al., 2000), some have not (Moore, 1987; Knapp and Moore, 1995). There have been recent studies suggesting that cortisol concentrations may not reflect human reactivity to stressful conditions in real life situations at all (Pollard, 1995). Plus there are some fish species whose glucocorticoid response is extremely muted and slow, although present (Barton and Vijayan, 2002). There are a number of reports that suggest that specific neuroendocrine responses are dependent on the specific stressor (Luo et al., 1994; Pacak et al., 1995, 1998; Romero and Sapolsky, 1996; Dhabar et al., 1997). Many investigators currently believe after substantial results have been collected from clinical, laboratory and field studies, that neuroendocrine stress responses are context dependent (Breuner and Hahn, 2000; Hayes, 2000; Carr et al., 2002; Carr and Summers, 2002; Greenberg, 2002; Greenberg et al., 2002; Wingfield and Kitaysky, 2002). However, specificity of response dependent on context and type of stressor may represent plasticity or flexibility of neuroendocrine stress machinery common to all stressors, rather than multiple systems set up for each stressor and each context. Plasticity in the timing of common responses is a reasonable mechanism to give flexibility that results in differential responses seen for various stressors and contexts. An example of flexibility of neuroendocrine response may be found in the lizard A. carolinensis (Korzan et al., 2000a, b). With respect to corticosterone secretion, two reports by Greenberg and colleagues left those investigators wondering whether social stress was enough to stimulate the HPA axis (Greenberg et al., 1984b; Greenberg and Crews, 1990). The first study showed a substantial increase in plasma corticosterone induced by social stress in subordinate males (Greenberg et al., 1984b). A more recent study, with a sampling regimen at 3 different and earlier time periods, did not produce any statistically significant elevations in corticosterone (Greenberg and Crews, 1990). Very recent work suggests that the corticosteroid response in A. carolinensis is extremely labile (Summers et al., 2002), implying that perhaps both earlier studies were accurate. Trying to infer a pattern of glucocorticoid response in A. carolinensis from an amalgam of these three studies, suggests a rapid increase in corticosterone secretion by ten minutes in both dominant and subordinate males in response to acute stress and aggression (Summers et al., 2002). This early response is very nicely correlated with an easily identifiable stressor. Very quickly, both males reduce corticosterone secretion to baseline levels. In the period that follows, from 40 min through a week or so, ensuing social interactions may stimulate elevated glucocorticoid responses from both dominant and subordinate males, but they are more likely and longer lasting in subordinate males (Sapolsky, 1983, 1989). During this time period elevated corticosterone was measured in subordinate males at 40 min (Summers et al., 2002), but not at one hour, one day, or one week (Greenberg and Crews, 1990) although there was a trend toward increases in both dominant and subordinate males. Although social aggression decreases during that period, the persistent nature of social stress for subordinate individuals may eventually lead to chronically elevated corticosterone, as was measured by Greenberg et al. at three weeks (1984b). Therefore, although there appear to be clearly defined acute and chronic phases of HPA axis activity, there are periods when sampling may not result in elevated glucocorticoids. It would be a mistake to suggest that social stress is absent during those periods when corticosteroid concentrations are not elevated.


Descriptions of stress responsiveness from the very beginning (Selye, 1936, 1937) have contrasted neuroendocrine secretion as acute versus chronic. Chronic stress responses are often viewed as maladaptive or pathological (Carr and Summers, 2002), and acute stress responses are more likely to be seen as adaptive, if not beneficial. However, all of the temporal manifestations of the stress response have important and adaptive behavioral consequences, which also influence the neuroendocrine machinery of the stress response (Summers, 2001).

Long-term temporal resolution and continuity of behavioral displays have not been quantified for Anolis, but it is clear that during social interaction aggression declines with time (Fig. 1). A look at display frequency during the first ten minutes of social interaction suggests a temporally bimodal distribution of aggressive acts for dominant (aggressive) males and also for subordinate (less aggressive) males. A significant decline in aggression at five minutes, suggests a period of reassessment, after which aggressive display by subordinate males decline.

Neuroendocrine responses to social stress also appear to be biphasic during the early and later phases of social interaction. Corticosterone concentrations in subordinate males peak twice during the first hour (Fig. 2), and then perhaps again much later (Greenberg et al., 1984b). The glucocorticoid response appears to be regulated, at least in part by central serotonergic activity (Abe and Hiroshige, 1974; Winberg et al., 1997a). In concert with HPA reactions, serotonergic activity of limbic structures increases by ten minutes in both dominant and subordinate males, followed by a secondary escalation in both, peaking at various times later during the period of social stress (Summers et al., 2002). It is the timing of the secondary increase in neuroendocrine activity that appears to be one way to distinguish dominant and subordinate social status.


There are two characteristics of serotonergic activity induced by social stress that are similar in dominant and subordinate males. A rapid increase in central serotonergic activity occurs in any male, and perhaps any female (Summers et al., 1997), A. carolinensis that engages in aggressive social interaction (Summers et al., 2002). How rapid is still unknown, but before 25 sec is a reasonable guess, as physical stress in A. carolinensis (Emerson et al., 2000), and social stress in Sceloporus jarrovi (Matter et al., 1998) enhance 5– HIAA/5-HT levels in this time frame (Summers, 2001). It seems likely that this early serotonergic activity, along with elevated plasma corticosterone, are responses to stress associated with novel aggression. During this early response period, through about ten minutes, dopaminergic and noradrenergic systems are also affected, but it is the serotonergic system activity that is most closely correlated with social and other stresses (Winberg and Nilsson, 1993a). Dominant and subordinate male serotonergic response to aggressive social interaction also similarly produce a secondary period of enhanced activity (Summers et al., 2002). The secondary serotonergic responses are not temporally similar, but offset.

Regardless of limbic region investigated, the secondary phase of enhanced serotonergic activity in subordinate male A. carolinensis is delayed compared with dominant males (Fig. 3). It is not surprising that monoaminergic activity is different in limbic regions based on social status, as prolonged subordination stress induces morphological changes in nucleus (Fuchs et al., 1995) and dendritic arbors (Margarinos et al., 1996) of hippocampal pyramidal cells, and also decreases binding of 5-HT transporters (McKittrick et al., 2000). In hippocampus (medial cortex) and nucleus accumbens dominant male A. carolinensis have secondary serotonergic peaks by 40 min of social interaction (Summers et al., 2002). Subordinate males do not have a second period of enhanced serotonergic activity until an hour in those regions, and peak activity is delayed until one week in medial amygdala-striatum.


The delay in enhanced serotonergic activity in the amygdalo-striatal region (posterior dorsal ventricular ridge plus paleostriatum; Greenberg, 1982; Bruce and Neary, 1995) is expressed in both dominant and subordinate male Anolis (Summers et al., 2002). The difference is that for dominant males the shift in peak activity is from 40 min for hippocampus or accumbens to an hour in medial amygdala-striatum, and in subordinate males the delay in serotonergic activity is much longer (Fig. 4). Serotonergic activity in mammalian amygdala stimulates the HPA axis (Feldman et al., 2000) via circuitry through the bed nucleus of the stria terminalis shared with the hippocampus (Herman and Cullinan, 1997; Herman and Ziegler, 2002). The hippocampus is an important site for negative feedback and inhibition of the HPA endocrine stress response (Sapolsky et al., 1984). Centrally and peripherally applied corticosterone stimulates serotonergic activity in the hippocampal cortex of A. carolinensis (Summers et al., 2000; Summers, 2001), so negative feedback may include a serotonergic component.

As hippocampal serotonergic activity occurs sooner, along with hippocampus being inhibitory for the HPA endocrine response, and because dominant male A. carolinensis have the most rapid hippocampal serotonergic response coupled with a lack of chronically elevated plasma corticosterone (Greenberg et al., 1984b; Greenberg and Crews, 1990), the hippocampus seems well suited to regulate short-term stress responses. On the other hand, serotonergic activity in amygdala stimulates HPA secretion (Feldman et al., 2000), serotonergic activity in anoline medial amygdala and striatum are delayed, and delayed in subordinate males to reasonably coincide with elevated corticosterone late (three weeks) in social cohabitation (Greenberg et al., 1984b). The evidence suggests that the processing of stress-related information occurs in a distributed fashion, with short-term regulation and inhibition of HPA activity controlled by hippocampus, and longer-term stimulation of HPA secretion associated with social subordination and the attendant behavior regulated by amygdala. The medial amygdala and ventral striatum are regions that regulate aggression and species specific social behavior in Anolis (Greenberg et al., 1979, 1984a, 1988; Greenberg, 1983). In this cooperative regulation scheme, these regions must relay current conditions between them, and there must be a mechanism to convert short-term reactions that facilitate more aggression into longer-term responsiveness that includes submissive behavior for subordinate animals.


As no animal is born dominant, the neuroendocrine machinery necessary for producing stress responses and the appropriate behavior for dominant status must be acquired. In addition, any individual may encounter an antagonist of greater or lesser social experience, ability and status each time an interaction takes place. Variation in neuroendocrine responsiveness appears to emanate, at least in part, from different social experience (Sapolsky, 1985; Knapp and Moore, 1996). Therefore, the neuroendocrine machinery necessary to produce appropriate behavioral responses must be easily modifiable (Summers, 2001). A plausible mechanism for both ontogenetic development and flexibility of the appropriate neuroendocrine machinery to handle the quick and variable responses necessary for varying social contexts, is simply the speed of the neuroendocrine stress response. A dominant male must always be alert and ready, and quicker to show aggressive intent, assess his opponent, and limit his opponent’s aggression if he is to be/remain dominant and to limit his own stress response (Summers, 2001). Rapidly limiting the stress response via the hippocampus presents the dominant male with behavioral opportunities uninhibited by chronically elevated corticosterone or 5-HT. Alertness, aggressive display, aggression, feeding and locomotion are all inhibited by 5-HT or corticosterone during social stress (Winberg et al., 1993a, b; Larson and Summers, 2001).


While neuroendocrine secretory products such as corticosterone and 5-HT influence behavior (Larson and Summers, 2001), behavior and social sign stimuli also influence neuroendocrine output (Korzan et al., 2000a, b, 2001, 2002). Specifically for Anolis, viewing aggression stimulates more aggressive activity (Yang et al., 2001), but it also influences central and plasma monoamine activity (Korzan et al., 2000a, b, 2001, 2002). In addition, eyespots appear to specifically stimulate the dopaminergic centers substantia nigra and ventral tegmental area (Korzan et al., 2001). When measured together nigral and tegmental dopaminergic, serotonergic and noradrenergic activity is elevated when a male views a mirrored reflection of himself as an opponent with darkened eyespots. The implication is that behavioral events, perhaps along with a genetic predisposition, are a part of the means by which the necessary neuroendocrine machinery is accrued during development of dominant characteristics and capacities, and during acquisition of dominance itself. It is unknown which kinds of experience may result in shorter latency to neuroendocrine response to stressors characteristic of dominant animals, but likely candidates include winning aggressive interactions, interactions with opponents without darkened eyespots, winning competition for food and mates, and successful copulations.


Social interaction is stressful for both dominant and subordinate males. However, the temporal resolution of neuroendocrine stress responses depends on social status, and appears to be an accurate measure of social status. Therefore, behavioral responses develop differently between dominant and subordinate males over time. Peripheral responses to stressful social stimuli, like glucocorticoids, may be attuned to social status at some times during social interaction, but do not always reflect the presence of social stress. Social stress is temporally biphasic, with bimodal behavioral and neuroendocrine responses. Serotonergic activity in response to social stress is attuned to temporal changes in behavior and status. That is, serotonergic activity is similar for dominant and subordinate males, but temporally offset. To regulate the temporally integrated and interactive set of neuroendocrine changes associated with social stress, different, but interactive regions of the brain appear to govern short-term and long-term stress. Faster neuroendocrine responses in males may permit behavioral adaptation for dominant social roles. Certain social interactions may result in faster neuroendocrine responses.


The symposium and resulting published works were funded by NIH grant R13 MH62670, NSF grant IBN #0100532, the Center for Biomedical Research Excellence (CoBRE) at the University of South Dakota on Neural Mechanisms of Adaptive Behavior, South Dakota EPSCoR, and the USD Office of Research. The data presented here represents contributions from numerous students, colleagues and collaborators, including Aaron Emerson, Neil Greenberg, Wayne J. Korzan, Earl T Larson, Christopher A. Lowry, John M. Matter, Jennifer McKay, Michael C. Moore, Aaron Prestbo, Kenneth J. Renner, Patrick J. Ronan, Tangi R. Summers, Gary R. Ten Eyck and Sarah Woodley. Work presented here was supported by NIH grants P20 RR15567 & NICHD-1-T32-HDO 7303-01A1, NSF grants IBN-9596009, OSR-9108773 & 9452894 & NSF EPSCoR Research Fellowship, HHMI grant 71195-539501, Nelson Foundation fellowship and grant, and Sigma Xi Grant-in-Aid of Research.

1 From the Symposium Stress-Is It More Than a Disease? A Comparative Look at Stress and Adaptation presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3– 7 January 2001, at Chicago, Illinois.


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