Review
The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms

https://doi.org/10.1016/j.neubiorev.2008.07.001Get rights and content

Abstract

Grooming is a widespread activity throughout the animal kingdom, but in primates (including humans) social grooming, or allo-grooming (the grooming of others), plays a particularly important role in social bonding which, in turn, has a major impact on an individual's lifetime reproductive fitness. New evidence from comparative brain analyses suggests that primates have social relationships of a qualitatively different kind to those found in other animal species, and I suggest that, in primates, social grooming has acquired a new function of supporting these. I review the evidence for a neuropeptide basis for social bonding, and draw attention to the fact that the neuroendrocrine pathways involved are quite unresolved. Despite recent claims for the central importance of oxytocin, there is equally good, but invariably ignored, evidence for a role for endorphins. I suggest that these two neuropeptide families may play different roles in the processes of social bonding in primates and non-primates, and that more experimental work will be needed to tease them apart.

Section snippets

What is grooming for?

Grooming, in primates as in most species, is all about physical touch. The actions are typically bimanual, involving sweeps with one hand interspersed with plucking movements by the other (Sparks, 1967). The plucking movements are directed at skin debris (scabs, skin flakes), spots, blemishes, and the occasional ectoparasite such as a tick or leech, or at vegetation caught in the fur. These movements have two particular characteristics: they are very rhythmic, and the plucking often involves

The social brain and the nature of primate relationships

Primates have unusually large brains for body size compared to other vertebrate groups, and over the past decade or so there has been considerable interest in why this should be. The consensus is now that the explanation lies in the complexity of primate social life. Originally proposed as the Machiavellian Intelligence Hypothesis (Byrne and Whiten, 1988), this was subsequently developed in quantitative form as the social brain hypothesis based on a demonstration that both social group and

The psychopharmacology of grooming

One of the striking behavioural features of grooming in those species that devote very substantial amounts of time to this activity is the fact that an animal who is being groomed can become so relaxed it can quite literally fall asleep. This seems to reflect the fact that social grooming has a number of physiological effects that include a reduction in the heart rate and a lowering of behavioural indices of stress (indexed as rates of scratching and yawning) (Goosen, 1981). Schino et al. (1988)

Discussion

Taken together, these findings suggest that oxytocin (but not vasopressin?) might function in a similar way to endorphins in producing a sense of calmness and contentedness. However, if so, it is far from clear what the causal sequence is here, since most of the circumstances that stimulate the production of oxytocin (mating, birth, breastfeeding, stroking) all involve mechanical stress, and are thus also likely to trigger the release of endorphins. Since neuroendocrines often operate in

References (96)

  • H. Kudo et al.

    Neocortex size and social network size in primates

    Anim. Behav.

    (2001)
  • J. Lehmann et al.

    Group size, grooming and social cohesion in primates

    Anim. Behav.

    (2007)
  • K.C. Light et al.

    More frequent partner hugs and higher oxytocin levels are linked to lower blood pressure and heart rate in premenopausal women

    Biol. Psychol.

    (2005)
  • F.L. Moore et al.

    Comparative neuroanatomy of vasotocin and vasopressin in amphibians and other vertebrates

    Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol.

    (1998)
  • E.E. Nelson et al.

    Brain structures of infant–mother attachment: contributions of opioids, oxytocin, and norepinephrine

    Neurosci. Biobehav. Rev.

    (1998)
  • R.J.M. Niesink et al.

    Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats

    Neuropharmacology

    (1989)
  • L.U. Sneddon

    The evidence for pain perception in fish: the use of morphine as an analgesic

    Appl. Anim. Behav. Sci.

    (2003)
  • G. Stefano et al.

    Endogenous morphine

    Trends Neurosci.

    (2000)
  • K. Uvnäs-Moberg

    Neuroendocrinology of the mother-child interaction

    Trends Endocrinol. Metab.

    (1996)
  • K. Uvnäs-Moberg

    Oxytocin may mediate the benefits of positive social interaction and emotions

    Psychoneuroendocrinology

    (1998)
  • J.M. van Ree et al.

    Low doses of β-endorphin increase social contacts of rats tested in dyadic encounters

    Life Sci.

    (1983)
  • D.M. Witt et al.

    Enhanced social interaction in rates following chronic, centrally infused oxytocin

    Pharmacol. Biochem. Behav.

    (1992)
  • R.M. Wittig et al.

    Focused grooming networks and stress alleviation in wild female baboons

    Hormones Behav.

    (2008)
  • L.J. Young

    Oxytocin and vasopressin receptors and species-typical social behaviors

    Horm. Behav.

    (1999)
  • H. Zacur et al.

    Galactorrhea-amenorrhea: psychological interaction with neuroendrocrine function

    Am. J. Obstet. Gynecol.

    (1976)
  • D.H. Abbott et al.

    Social suppression of reproduction in subordinate talapoin monkeys, Miopitehcus talapoin

  • J. Altmann

    Baboon Mothers and Infants

    (1980)
  • J.A. Amico et al.

    Anxiety and stress responses in female oxytocin deficient mice

    J. Neuroendocrin.

    (2004)
  • A. Argioglas et al.

    Central function of oxytocin

    Neurosci. Biobehav.

    (1991)
  • A. Aron et al.

    Inclusion of other in the self scale and the structure of interpersonal closeness

    J. Pers. Soc. Psych.

    (1992)
  • L. Barrett et al.

    The utility of grooming in primate troops

  • R.A. Barton

    Grooming site preferences in primates and their functional significance

    Int. J. Primatol.

    (1985)
  • R.A. Barton et al.

    Evolution of the social brain

  • J.D. Belluzzi et al.

    Enkephalin may mediate euphoria and drive-reduction reward

    Nature

    (1977)
  • I.F. Bielsky et al.

    Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice

    Psychoneuroendocrinology

    (2004)
  • M.L. Boccia

    A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys

    Int. J. Primatol.

    (1983)
  • J.L. Bottoroff

    The use and meaning of touch in caring for patients with cancer

    Oncol. Nurs. Forum

    (1993)
  • L.A. Bowman et al.

    Suppression of oestrogen-induced LH surges by social subordination in talapoin monkeys

    Nature

    (1978)
  • K.D. Broad et al.

    Mother-infant bonding and the evolution of mammalian social relationships

    Phil. Trans. R. Soc. Lond.

    (2006)
  • M. de L. Brooke

    The effect of allopreening on tick burdens on moulting eudyptid penguins

    Auk

    (1985)
  • J.K. Burgoon

    Relational message interpretations of touch, conversational distance and posture

    J. Nonverbal Behav.

    (1991)
  • J.K. Burgoon et al.

    Interpretations, evaluations, and consequences of interpersonal touch

    Human Commun. Res.

    (1992)
  • Byrne, R.W. Whiten, A. (Eds.), 1988. Machiavellian Intelligence. Oxford University Press,...
  • R.W. Byrne et al.

    Neocortex size predicts deception in primates

    Proc. R. Soc. Lond.

    (2004)
  • C.S. Carter et al.

    Physiological substrates of mammalian monogamy: the prairie vole model

    Neurosci. Biobehav.

    (1995)
  • M.M. Cho et al.

    The effects of oxytocin and vasopressin on partner preference in male and female voles (Microtus ochrogaster)

    Behav. Neurosci.

    (1999)
  • S. Datta

    Relative power and the maintenance of rank

  • R.A. Depue et al.

    A neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation

    Behav. Brain Sci.

    (2005)
  • Cited by (541)

    View all citing articles on Scopus
    View full text