Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 Oct 7;271(1552):2077–2084. doi: 10.1098/rspb.2004.2831

Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep.

Ana P da Costa 1, Andrea E Leigh 1, Mei-See Man 1, Keith M Kendrick 1
PMCID: PMC1691828  PMID: 15451699

Abstract

Faces are highly emotive stimuli and we find smiling or familiar faces both attractive and comforting, even as young babies. Do other species with sophisticated face recognition skills, such as sheep, also respond to the emotional significance of familiar faces? We report that when sheep experience social isolation, the sight of familiar sheep face pictures compared with those of goats or inverted triangles significantly reduces behavioural (activity and protest vocalizations), autonomic (heart rate) and endocrine (cortisol and adrenaline) indices of stress. They also increase mRNA expression of activity-dependent genes (c-fos and zif/268) in brain regions specialized for processing faces (temporal and medial frontal cortices and basolateral amygdala) and for emotional control (orbitofrontal and cingulate cortex), and reduce their expression in regions associated with stress responses (hypothalamic paraventricular nucleus) and fear (central and lateral amygdala). Effects on face recognition, emotional control and fear centres are restricted to the right brain hemisphere. Results provide evidence that face pictures may be useful for relieving stress caused by unavoidable social isolation in sheep, and possibly other animal species, including humans. The finding that sheep, like humans, appear to have a right brain hemisphere involvement in the control of negative emotional experiences also suggests that functional lateralization of brain emotion systems may be a general feature in mammals.

Full Text

The Full Text of this article is available as a PDF (470.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albert D. J., Walsh M. L. Neural systems and the inhibitory modulation of agonistic behavior: a comparison of mammalian species. Neurosci Biobehav Rev. 1984 Spring;8(1):5–24. doi: 10.1016/0149-7634(84)90017-4. [DOI] [PubMed] [Google Scholar]
  2. Bartels A., Zeki S. The neural basis of romantic love. Neuroreport. 2000 Nov 27;11(17):3829–3834. doi: 10.1097/00001756-200011270-00046. [DOI] [PubMed] [Google Scholar]
  3. Bartels Andreas, Zeki Semir. The neural correlates of maternal and romantic love. Neuroimage. 2004 Mar;21(3):1155–1166. doi: 10.1016/j.neuroimage.2003.11.003. [DOI] [PubMed] [Google Scholar]
  4. Broad K. D., Hinton M. R., Keverne E. B., Kendrick K. M. Involvement of the medial prefrontal cortex in mediating behavioural responses to odour cues rather than olfactory recognition memory. Neuroscience. 2002;114(3):715–729. doi: 10.1016/s0306-4522(02)00231-2. [DOI] [PubMed] [Google Scholar]
  5. Broad K. D., Mimmack M. L., Kendrick K. M. Is right hemisphere specialization for face discrimination specific to humans? Eur J Neurosci. 2000 Feb;12(2):731–741. doi: 10.1046/j.1460-9568.2000.00934.x. [DOI] [PubMed] [Google Scholar]
  6. Da Costa A. P., Broad K. D., Kendrick K. M. Olfactory memory and maternal behaviour-induced changes in c-fos and zif/268 mRNA expression in the sheep brain. Brain Res Mol Brain Res. 1997 Jun;46(1-2):63–76. doi: 10.1016/s0169-328x(96)00272-0. [DOI] [PubMed] [Google Scholar]
  7. Edwards Jane, Jackson Henry J., Pattison Philippa E. Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clin Psychol Rev. 2002 Jul;22(6):789–832. doi: 10.1016/s0272-7358(02)00130-7. [DOI] [PubMed] [Google Scholar]
  8. George M. S., Huggins T., McDermut W., Parekh P. I., Rubinow D., Post R. M. Abnormal facial emotion recognition in depression: serial testing in an ultra-rapid-cycling patient. Behav Modif. 1998 Apr;22(2):192–204. doi: 10.1177/01454455980222007. [DOI] [PubMed] [Google Scholar]
  9. Haxby JV, Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends Cogn Sci. 2000 Jun;4(6):223–233. doi: 10.1016/s1364-6613(00)01482-0. [DOI] [PubMed] [Google Scholar]
  10. Kendrick K. M., da Costa A. P., Leigh A. E., Hinton M. R., Peirce J. W. Sheep don't forget a face. Nature. 2001 Nov 8;414(6860):165–166. doi: 10.1038/35102669. [DOI] [PubMed] [Google Scholar]
  11. Macdonald H., Rutter M., Howlin P., Rios P., Le Conteur A., Evered C., Folstein S. Recognition and expression of emotional cues by autistic and normal adults. J Child Psychol Psychiatry. 1989 Nov;30(6):865–877. doi: 10.1111/j.1469-7610.1989.tb00288.x. [DOI] [PubMed] [Google Scholar]
  12. Markowitsch Hans J. Differential contribution of right and left amygdala to affective information processing. Behav Neurol. 1998;11(4):233–244. doi: 10.1155/1999/180434. [DOI] [PubMed] [Google Scholar]
  13. Morris J. S., Frith C. D., Perrett D. I., Rowland D., Young A. W., Calder A. J., Dolan R. J. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature. 1996 Oct 31;383(6603):812–815. doi: 10.1038/383812a0. [DOI] [PubMed] [Google Scholar]
  14. Morton J., Johnson M. H. CONSPEC and CONLERN: a two-process theory of infant face recognition. Psychol Rev. 1991 Apr;98(2):164–181. doi: 10.1037/0033-295x.98.2.164. [DOI] [PubMed] [Google Scholar]
  15. Parrott R. F., Misson B. H., de la Riva C. F. Differential stressor effects on the concentrations of cortisol, prolactin and catecholamines in the blood of sheep. Res Vet Sci. 1994 Mar;56(2):234–239. doi: 10.1016/0034-5288(94)90109-0. [DOI] [PubMed] [Google Scholar]
  16. Peirce Jonathan W., Kendrick Keith M. Functional asymmetry in sheep temporal cortex. Neuroreport. 2002 Dec 20;13(18):2395–2399. doi: 10.1097/00001756-200212200-00004. [DOI] [PubMed] [Google Scholar]
  17. Perry R. J., Rosen H. R., Kramer J. H., Beer J. S., Levenson R. L., Miller B. L. Hemispheric dominance for emotions, empathy and social behaviour: evidence from right and left handers with frontotemporal dementia. Neurocase. 2001;7(2):145–160. doi: 10.1093/neucas/7.2.145. [DOI] [PubMed] [Google Scholar]
  18. Ross E. D., Orbelo D. M., Cartwright J., Hansel S., Burgard M., Testa J. A., Buck R. Affective-prosodic deficits in schizophrenia: comparison to patients with brain damage and relation to schizophrenic symptoms [corrected]. J Neurol Neurosurg Psychiatry. 2001 May;70(5):597–604. doi: 10.1136/jnnp.70.5.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Thomas K. M., Drevets W. C., Dahl R. E., Ryan N. D., Birmaher B., Eccard C. H., Axelson D., Whalen P. J., Casey B. J. Amygdala response to fearful faces in anxious and depressed children. Arch Gen Psychiatry. 2001 Nov;58(11):1057–1063. doi: 10.1001/archpsyc.58.11.1057. [DOI] [PubMed] [Google Scholar]
  20. Transmission of AIDS virus. Science. 1987 Dec 11;238(4833):1497–1497. [PubMed] [Google Scholar]
  21. Vellucci S. V., Parrott R. F., da Costa A. C., Ohkura S., Kendrick K. M. Increased body temperature, cortisol secretion, and hypothalamic expression of c-fos, corticotrophin releasing hormone and interleukin-1 beta mRNAs, following central administration of interleukin-1 beta in the sheep. Brain Res Mol Brain Res. 1995 Mar;29(1):64–70. doi: 10.1016/0169-328x(94)00230-c. [DOI] [PubMed] [Google Scholar]
  22. Zald David H. The human amygdala and the emotional evaluation of sensory stimuli. Brain Res Brain Res Rev. 2003 Jan;41(1):88–123. doi: 10.1016/s0165-0173(02)00248-5. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES