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

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.

Behavioural and neurophysiological evidence for face identity and face emotion processing in animals

“…However, we have shown that female sheep exhibit specific preferences for the faces of individual males independent of social familiarity with them (Kendrick et al 1995). In addition, simple exposure to face pictures of sheep of the same breed (but unfamiliar individuals) reduces behavioural, autonomic and endocrine indices of stress caused by social isolation (da Costa et al 2004).…”

Dominance and stress signalling of carotenoid pigmentation in Arctic charr (Salvelinus alpinus): Lateralization effects?

“…Earlier reports have provided some evidence for behavioural lateralization in stress responses [24,28], and that is mainly processed by the right brain hemisphere in mammals [24]. For instance, in sheep social isolation stress is reduced by familiar faces and leads to increased activity in the right hemisphere [51], and strongly lateralized mothers had higher stress response than weakly lateralized mothers following separation from their young [52]. Further, stress induced temperature elevation in the right ear, corresponding to the right hemisphere, has been reported in marmosets [53] and cats [54].…”

MRI Techniques and New Animal Models for Imaging the Brain

“…In large animals, such as sheep or pigs, similar neurobiological factors have been found to be involved in emotional responses, especially in stressful situations. Invasive neurobiological approaches based on functional neuroanatomy (sheep: da Costa et al 2004, Rivalland et al 2007, Vellucci & Parrott 1994, intracerebroventricular pharmacology (pigs: Johnson et al 1994, Salak-Johnson et al 2004, and neurochemical brain content (e.g. in pigs, Kanitz et al 2003, Loijens et al 2002, Piekarzewska et al 1999, Piekarzewska et al 2000, Zanella et al 1996 have demonstrated the involvement of neuropeptides such as CRF and enkephalins in different brain areas including the hypothalamus, brainstem and cortices.…”