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).
DISCUSSION
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.
