mise à jour du
21 janvier 2007
Neurobiol Aging
Aging, dominance history, and social behavior
in Java-monkeys (Macaca fascicularis)
Veenema HC, Spruijt BM, Gispen WH, van Hooff JA.
Ethology and Socio-ecology, Department of Comparative Physiology
Utrecht University, The Netherlands


Abstract : The aim of this study was to investigate the influence of the dominance history of socially housed Java-monkeys on the aging process. In monkeys, social subordinance is generally associated with elevated levels of cortisol, which, in turn, have been suggested to influence cognitive decline. As cognitive skills are necessary for successful social life, we investigated the effect of old age in relation to the dominance history of the animals on their social behavior by comparing old females with their younger daughters. Old age, especially in combination with a history of low rank, led to a withdrawal from social interactions with unfamiliar animals and to a decrease in amounts of aggression received. Still, however, old animals showed an increase in behaviors associated with arousal. A reduced ability to deal with complex social interactions, caused by a decline in information processing abilities, is suggested as an explanation for these results.

Several studies have shown that aged primates are impaired on a variety of learning tasks, e.g., delayed response and delayed non-matching-to-sample tasks (10,33,37,38). Most studies, however, report large individual variation in performance within the aged group for the various tasks. For example, in the study of Rapp and Amaral (38) only a subgroup of six aged monkeys (Macaca mulatta) showed significant impairment in performance on a delayed non-matching-to-sample task, whereas three other aged monkeys did not differ from the young control group. Similar reports of individual variation are known from studies with aged humans (1,23) and aged rats (e.g., ref. 18).
A differential exposure to events or processes during life that influence the degree of cognitive deterioration later in life may explain this individual variation. Investigations by Jolles et al. (23) suggest that for humans the amount of biological life events such as head injuries, anesthesia, or use of alcohol or medicines partly explains individual variation between aged individuals. These small events may accumulate during life and result in a decline in cognitive performance. Another process that influences cognitive decline is the amount of stress a subject experiences during life.
Evidence for neurotoxic effects of glucocorticoids was first found by Landfield et al. (26) in male rats. Elevated levels of glucocorticoids disturb the calcium homeostasis in brain areas that are involved in cognitive processes (27) and prolonged exposure to these elevated levels can lead to cell dysfunction or cell deathe in these areas (for reviews, see refs. 24 and 25). This effect of elevated levels of corticosteroids has been confirmed for several animals species. In the tree shrew, changes in the cytoskeletal structure of hippocampal neurons were observed in relation to elevated levels of cortisol (17).
In rats, Sapolsky et al. (43) found an influence of glucocorticoids on neuronal death in the hippocampus; this effect has been confirmed for the primate brain (vervet monkeys, Cercopithecus aethiops) by Uno et al. (51). This suggests that differences between individuals in the amount of stress experienced during life can explain differences in cognitive abilities between these individuals later in life (cf. 40, 49). To study the relationship between prolonged periods of stress and changes in cognitive abilities later in life, socially living primates, such as long-tailed macaques, may provide an excellent model. Social life in these macaques results in long-term differences between individuals in levels of psychosocial stress. Longtailed macaques living in a social group are known to have a strict dominance hierarchy. In these social groups, female members of the same family hold similar dominance positions and support each other against lower-ranking families. This results in a dominance hierarchy that remains stable often for the entire life of an adult individual (53). Low ranking monkeys receive mor aggression, fewer support and receive fewer affinitive gestures than high-ranking animals (see ref. 31). In general, they have more difficulty in obtaining access to resources such as food or mating partners, which can result in lower reproductive success for low-ranking monkeys (see ref. 47).
Although some animals may cope more successfully with their social position than others (44), there is a general trend for a relationship between dominance position and basal stress levels. For vervet monkeys, Uno et al. (51) found indications that socially subordinate animals had been subjected to social stress and suffered from multiple gastric ulcers. Low dominance position led to increased levels of cortisol in wild male baboons (Papio anubis) (41, 42), in captive long-tailed macaques (54), and in a stable group of captive female rhesus monkeys (20). Thus, in a situation where the dominance position of an animal has been stable for a considerable amount of time, the rank of the animal may be used as an indicator for the total amount of psychosocial stress this animal has experienced.
Another advantage of studying socially living macaques is that this creates the possibility to use social behavior as a measure for aging. Higher cognitive abilities are believed to have evolved at least partly in response to the challenges of interacting with conspecifics, which implies that animals can only be successful in their social life when these abilities are intact (11). Many different cognitive abilities are used in social life, and even changes in only some of these abilities will have their impact on the social behavior of the animals. Monkeys recognize other animals individually, they know their social relation to these animals, and data also shows that they even understand the relationships between other animals (5,11,13). With this information they can use different behavioral strategies to cope with social situations that might influence their dominance position (e.g., 11,15,19). Some of the strategies that have been described are reconciliation of conflicts by affiliating with an opponent, redirecting aggression towards lower-ranking animals (6,8), or attacking the family members of an animal by which they were attacked (5).
This suggests that the cognitive abilities used by an individual in social interactions range from attending relevant clues in the behavior of others, memorizing and recalling past actions by conspecifics, predicting their future actions, and adjusting its own behavior in response. If, with increasing age, some of these cognitive abilities decline, then animals may have more difficulty using adequate strategies. Studies that investigated the effects of aging on the social behavior of macaques have reported a withdrawal of old animals from social interactions with other group members (21,29,30,34,35,39). Combining the facts that aging results in a decline of cognitive abilitie and that cognitive abilities are important for successful social life, we infer that cognitive decline may be one of the factors in the process of social withdrawal.
In this study we investigated the effect of dominance history on age-related changes in social behavior. If dominance history influences the aging process, this should result in more pronounced changes in behavior with age in low-ranking animals. Similarly, we expect that if animals have more difficulty in using adequate behavioral strategies, they will show more behaviors associated with acute stress (scratching, yawning, body shake, auto-grooming, cf. 28).
In this study we find a clear effect of age on activity patterns, social behavior, aggression received, and stress-related behaviors. Old age led to a withdrawal from grooming interactions with unrelated animals and to a decrease in total time spent in social contact. These findings are in agreement with the results of other studies that old age in macaques leads to social withdrawal (21,29,30,34,35,39).
However, age-related changes in social behavior were influenced by rank as well. Our results show that the effect of age on social withdrawal gradually becomes stronger when families are lower in rank, i.e., old animals belonging to high-ranking families showed almost no signs of social withdrawal, whereas the effect of age on social withdrawal was strongest in the lowest-ranking families. The total time sitting follows the same pattern, which in combination with the previous result indicates that old animals, especially when they are low in rank, have a greater tendency to sit alone without having social interactions. These results agree with our predictions that a history of social subordination (and hence psychosocial stress) results in a stronger effect of age on changes in social behavior.
Hauser and Tyrell (21) suggested that physiological deterioration could be an explanation for the social withdrawal they observed. This explanation could apply to the changes in locomotion and resting patterns, which are probably the best indicators of physiological deterioration. However, because we do not find an effect of rank on the age-related changes in locomotion and resting, physiological deterioration is probably not sufficient to explain the changes in social behavior, where we do find this influence of rank. It could be argued that the stronger social withdrawal in old low-ranking animals is not an effect of old age and a history of low dominance, but merely represents an adaptive strategy of lowranking animals to avoid aggression and to find safer places in the group. However, this explanation seems unlikely for two reasons.
First, the social withdrawal is not present in young low-ranking adults and only slowly develops with increasing age. Both young and old low-ranking animals would benefit from preventing aggression and should avoid higher-ranking animals to the same extent. Second, one could question whether avoiding social contact and becoming more peripheral indeed provides more safety. One of the reasons for macaques to live in groups is safety from predators (12,45). Although there are no predators in captivity, the tendency to remain in close proximity with other animals is probably under strong genetic control and selected for by natural selection. Still, a similar pattern of stronger social withdrawal in old low-ranking long-tailed macaques was observed in a study on wild long-tailed macaques by van Noordwijk and van Schaik (36). Low-ranking animals became peripheral at an earlier age than high-ranking ones. They also disappeared from the study site (and most probably died) at an earlier age.
This evidence shows that preventing aggression by becoming peripheral is not a good strategy and jeopardizes survival. Therefore, other factors must play a role in the pattern of social withdrawal. We suggest that the stronger social withdrawal in low-ranking animals results from a stronger degeneration of cognitive abilities in low-ranking animals. Through elevated levels of social stress, dominance history may have influenced age-related changes in the brain and thus reduced the ability to cope with complex social interactions. In this way, old individuals with a long history of low rank would not actively choose to live at the periphery of the group, but would be forced into this situation because of their inability to perform adaptive social behavior necessary for maintaining a central position in the group. Our data shows that aged animals still have normal relationships with members of their family, and that they have a preference for social contact with other old animals over younger individuals. Both groups of animals are more familiar to the old individuals and may therefore be more predictable in their behavior or pose less of a threat to the old individuals.
One question that remains, however, is why the effect of age on rates of scratching, yawning, and body-shake is not stronger in low-ranking animals than in high-ranking ones. Although the increase with age in these behaviors seems to indicate that older animals experience more stress, the changes in these behaviors do not follow the same pattern as the social withdrawal. The explanation probably lies in the fact that these behaviors are associated with acute stress experienced in certain situations such as aggressive interactions (7,14,28).
Because our results show that aging leads to a large variability in patterns of social behavior that are influenced by dominance history as well, these measures of acute stress should be related to the number and type of social interactions the animals still have. If animals show a strong social withdrawal from certain type of interactions (e.g., interactions with young unrelated animals) but still have some of these interactions, one would predict differences in behavior during these interactions from behavior during interactions from which they do not withdraw (e.g., with old group-members, or with their own family. Our results on the change in partner preferences towards animals that are more familiar suggests that older animals may prefer a more predictable environment. Changes in the predictability of the behavior can be investigated by means of sequential analysis.
Two studies have shown that old age leads to differences in structure of behavior. In rats, Spruijt (48) showed a progressive decline in social attention in aged rats by using a sequential analysis. In interactions with a social partner, young rats were more predictable on the basis of the partner's behavior than on their own behavior, but this pattern gradually changed with age and old rats became more predictable on the basis of their own behavior than on the basis of the behavior of their partner. A similar experiment was done by Fitts (16) with monkeys, and the results were comparable; old monkeys were more predictable on the basis of their preceding behavior than young monkeys. These results indicate that the reason why aged animals change their preference toward members of the same age of the same family may be related to the predictability in behavior of the partner.
This is another indication that information processing abilities decline with age and that this effect is stronger in low-ranking animals. However, in order to obtain more evidence for this hypothesis, a closer examination of the social interactions of old animals is needed.

Neurobiol Aging. 2001 Mar-Apr;22(2):273-81.
Increased rigidity with age in social behavior of Java-monkeys (Macaca fascicularis).
Veenema HC, van Hooff JA, Gispen WH, Spruijt BM.
In this study we investigated the effect of aging on the structure of behavior of socially housed Java-monkeys. Indices of the sequential structure of an animal's own ongoing behavior and of its responses to behavior of other animals were calculated using an information statistic approach. These indices reflect information-processing abilities of an animal, as they represent the ability of an animal to adjust its behavior in response to actions by interaction partners. The influence of an animal's dominance history on the age-related changes was investigated as well. In the literature social subordinance in monkeys is generally associated with elevated levels of cortisol which, in turn, have been suggested to influence information processing abilities. In this study, old animals of low dominance history became more rigid in their own ongoing behavior, whereas old animals of high dominance history did not differ from young animals. The ability of old animals to maintain normal levels of predictability during social interactions declined, but only in social interactions with unfamiliar animals, such as young or unrelated animals. These results may explain the generally found social withdrawal of old non-human primates.

J Comp Psychol. 1997 Mar;111(1):91-9.
Differential kinship effect on reconciliation in three species of macaques (Macaca fascicularis, M. fuscata, and M. sylvanus).
Aureli F, Das M, Veenema HC.
Yerkes Regional Primate Research Center, Emory University, Atlanta, Georgia, USA.
Macaque societies are typically characterized by despotic dominance styles and strong bonds between related individuals. Interspecies variation in dominance style, however, has been recently documented. This study investigated whether kinship effects on social interactions vary depending on the species dominance style. Reconciliation was chosen as as a measure of relationship quality between group members. Groups of Japanese (Macaca fuscata) and long-tailed (M. fascicularis) macaques were selected for their highly despotic style, and Barbary (M. sylvanus) macaques were chosen for their lower level of despotism. The findings confirmed the hypothesis that kinship effects on reconciliation are stronger the more despotic the species is. Barbary macaque nonkin reconciled more often than nonkin of the other 2 species. In addition, the differences in reconciliation frequency between kin and nonkin were less pronounced among the less despotic Barbary macaques.

Hormones and Behavior 2007;51(1):11-19
Low inborn anxiety correlates with high intermale aggression: Link to ACTH response and neuronal activation of the hypothalamic paraventricular nucleus
Alexa H. Veenema , Luz Torner, Annegret Blume, Daniela I. Beiderbeck, Inga D. Neumann
Aggression constitutes a central problem in several psychopathologies, including anxiety and depression disorders and antisocial behaviors. In particular, the activity of the hypothalamic&endash;pituitary&endash;adrenocortical (HPA) axis has been associated with aggression-related disorders. The present study assessed whether genetically determined levels of anxiety-related behavior influence the level of intermale aggression and whether this is associated with differences in neuroendocrine responsiveness and neuronal activation in the brain. Adult male Wistar rats bred for high (HAB) or low (LAB) anxiety-related behavior were used, as well as non-selected rats (NAB) with an intermediate anxiety level. LAB residents displayed more aggressive behavior than HAB and NAB residents during the resident&endash;intruder (RI) test. Moreover, an inverse correlation was found between the level of anxiety and the level of aggression. The plasma corticotropin (ACTH) response to RI-test exposure was significantly higher in LABs than in HABs and NABs, indicating that a higher level of aggression was linked to an elevated hormonal stress response. Furthermore, LAB residents showed more neuronal activation in the parvocellular part of the hypothalamic paraventricular nucleus (PVN) than HAB residents 1 h after the RI-test. In addition, a tendency toward a higher number of c-Fos-positive cells in LABs compared with HABs was observed in the medial amygdala, hypothalamic attack area and central amygdala, areas relevant for the regulation of aggression. These data demonstrate that low trait anxiety is correlated with high intermale aggression. Furthermore, the increased neuronal activation of the PVN along with the higher ACTH responsiveness might underlie the display of high aggression.

Tous les travaux de B. Deputte