NATURE NEUROSCIENCE VOLUME 15 | NUMBER 5 | MAY 2012 681
Decades of animal research have provided a rich account of neuroendo-
crinological influences on the social behavior of non-human animals.
Inspired by these findings, human social neuroendocrinological
research has flourished in recent years. Nevertheless, seemingly
contradictory data, multi-leveled interactions and methodological
hurdles have raised serious challenges. Here we summarize important
findings in animal and human social neuroendocrinology, focusing
on how roots in animal research have sprung new branches of human
research. We then outline ways in which human research can con-
tinue to profit from the methods and discoveries of animal research
and ways in which human research offers unique opportunities for
increasing our understanding of the social cognitive, affective and
motivational processes underlying social neuroendocrinology.
The neuroendocrinology of animal social behavior
Neuropeptides (that is, oxytocin and arginine vasopressin, AVP) and
steroid hormones (that is, testosterone and estradiol) have a central
role in the social lives of animals. As comprehensive reviews on
animal social neuroendocrinology have appeared recently
1–3
, we will
only briefly touch on themes in this literature that have provided the
roots for research in humans (Fig. 1). With that in mind, we focus on
oxytocin, AVP and testosterone and their influences on four general
categories: affiliation, social cognition, aggression and anxiety/stress
responses. Although other hormones (such as estradiol) are important
for animal social behavior, their effects on human social behavior are
not well explored and will therefore not be reviewed here.
Oxytocin and AVP perform social functions in a wide variety of
species
2
and show remarkable evolutionary preservation of struc-
ture and function
4
. Oxytocin has proven to be particularly critical
for the expression of affiliative behaviors. Its involvement in mater-
nal behavior is well established
2
. It also determines whether or not
individuals of various rodent species engage in alloparental behav-
ior
5
, the parenting of non-offspring. Oxytocin is also important
for pair bonding and partner preference in a number of species.
In prairie voles, a rodent that exhibits unusually monogamous pat-
terns of behavior, oxytocin increases females’ preference for spe-
cific partners and oxytocin antagonists decrease that preference
6
.
Accordingly, extracellular concentrations of oxytocin increase (in
the nucleus accumbens, NAcc) during mating in females and during
parturition
7
. It is important to note that much of oxytocin function,
particularly in regards to affiliative behaviors, is regulated by estro-
gen’s influence on the expression of its receptors
8
.
Mother-offspring bonding, pair bonding and partner preferences
all rely on the ability of the animal to form a memory of the offspring
or partner. Oxytocin is important for social memory in a variety of
species
9
, determining scent-based memory in animals that rely on
scents to identify conspecifics. It appears to be particularly important
for the acquisition of social memories. Rats with a null mutation in
their oxytocin gene, for example, regain social memory if they receive
oxytocin centrally before their initial encounter with a target animal
10
.
It may also facilitate maternal memory consolidation
11
.
Oxytocin is not usually associated with aggression per se, although
it appears to be involved in maternal aggression
12
. Finally, oxytocin
moderates physiological stress responses and anxious behavior. In ham-
sters, for example, high cortisol levels inhibit wound healing such that
wound size is a gauge of the stress response and its effect on the body;
oxytocin administration buffers the stress response such that wound
size is decreased for isolated animals, whereas a centrally delivered
oxytocin antagonist impairs wound healing in paired animals
13
. Data
also demonstrate its anxiolytic qualities. Mice lacking the oxytocin gene
exhibit more anxious behavior in their exploration of mazes
14
.
AVP also affects affiliative behaviors
15
. In rats, AVP is implicated in
paternal behaviors, such as grooming, crouching over and contacting
pups
16
. AVP is also important for partner preference and pair bond-
ing, particularly for males in a variety of species. Central adminis-
tration of AVP in prairie vole males who have not mated triggers a
selective preference for mates
15
. The distribution of AVP receptors in
The animal and human neuroendocrinology of social
cognition, motivation and behavior
Cade McCall & Tania Singer
Extensive animal and recent human research have helped inform neuroendocrinological models of social cognition, motivation and
behavior. In this review, we first summarize important findings regarding oxytocin, arginine vasopressin and testosterone in the
domains of affiliation, social cognition, aggression and stress/anxiety. We then suggest ways in which human research can continue to
profit from animal research, particularly by exploring the interactive nature of neuromodulatory effects at neurochemical, organismic
and contextual levels. We further propose methods inspired by the animal literature for the ecologically valid assessment of affiliative
behavior in humans. We conclude with suggestions for how human research could advance by directly assessing specific social
cognitive and motivational mechanisms as intermediate variables. We advocate a more comprehensive look at the distinct networks
identified by social neuroscience and the importance of a motivational state, in addition to approach and avoidance, associated with
quiescence and homeostatic regulation.
Max Planck Institute for Human Cognitive and Brain Sciences, Department of
Social Neuroscience, Leipzig, Germany. Correspondence should be addressed
to T.S. (singer@cbs.mpg.de).
Published online 15 April 2012; doi:10.1038/nn.3084
FOCUS ON SOCIAL NEUROSCIENCE
REVIEW
npg
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