Neurobiological correlates of visual and olfactory recognition in sheep

Abstract

This paper describes neurophysiological and behavioural experiments which investigate the ability of sheep to recognise different individuals using visual and olfactory cues. Behavioural experiments using Y-mazes with back-projected images of faces have shown that sheep can distinguish between the faces of sheep and humans when the faces are presented in a frontal view although they have more difficulty in doing so if the faces are presented in profile, upside down or with the eyes obscured. Single-cell electrophysiological recordings made from neurones in the temporal cortex have shown that sheep, like non-human primates, have cells in this region that code preferentially for facial stimuli and that their responses are also diminished or abolished if the faces are presented upside-down, in profile, or with the eyes obscured. Different sub-populations of cells code for faces of similar social and emotional significance. Thus one population of cells codes for faces with horns and their responses are also modulated by the size of the horns, another population codes for faces of animals of the same breed, and particularly familiar animals, and a final population codes for faces of humans and dogs. Visual cues from body shape and posture are also important for recognition of different classes of individual. Field studies have shown that sheep find it difficult to recognise humans approaching them if they change their posture to quadrupedal as opposed to a bipedal one. Electrophysiological studies have also demonstrated the presence of cells in the temporal cortex which respond preferentially to the sight of a human body shape and their activity is influenced by body orientation, posture and direction of movement. In some cases alterations to the human's appearance can also influence their activity. Olfactory recognition studies have used electrophysiological, in vivo sampling and behavioural analyses to establish the mechanisms whereby a maternal ewe develops the ability to selectively recognise the odour signatures of its own lambs within the first few hours of giving birth. Electrophysiological recordings from mitral cells in the olfactory bulb have shown that none of them respond preferentially to lamb odours pre-partum, when the ewes show no interest in lambs, whereas 60% of them do so after ewes have bonded with their lambs. A sub-population of mitral cells also responds differentially to own and alien lamb odours post-partum. Neurochemical studies have shown that lamb odours do not evoke transmitter release within the olfactory bulb pre-partum whereas, post-partum, own lamb odours stimulate release of the intrinsic amino acid transmitters, GABA and glutamate whereas both own and alien lamb odours evoke equivalent increases in the release of the centrifugal pathway transmitters, acetylcholine and nonadrenaline. Overall these experiments provide compelling evidence that the sheep, which is after all a social animal, makes use of sophisticated visual cues from the face and body and of olfactory cues from the body and wool to recognise different individuals. The neural pathways which are involved in both of these recognition processes also show remarkable evidence of plasticity. However, there appears to be a much closer link between recognition and emotional significance demonstrated in the coding strategies employed by the neural circuits involved in individual recognition in the sheep brain compared to that of a primate and, indeed, they seem to be organised more for identifying a small number of different categories of individuals rather than for a large number of individuals per se. It is possible therefore that social evolutionary pressures to specifically identify large numbers of individuals of similar emotional significance has been achieved by weakening the organisational influence of affect on coding strategies of cells in the temporal cortex in favour of a more extensive feature detection system allowing accurate discrimination between a large number of individuals and their expressions under a number of different viewing conditions.