Neural Encoding Principles in Face Perception Revealed Using Non-Primate Models

Specialised neural systems for encoding faces and face emotion cues have been found in sheep which are very similar to those described in human and non-human primates. Sheep exhibit highly sophisticated face identity and face emotion discrimination skills, use configural cues and also have a right hemisphere dominance in face processing. Various neuroanatomical approaches have identified the different brain regions involved and electrophysiological recording methods have established some of the encoding strategies utilised, particularly in the temporal and frontal cortices. Increasingly, these electrophysiological studies are moving into multiarray recording strategies and being used to inform computational and modelling approaches. This chapter will provide an overview of what we know from studies on sheep about the neural substrates involved in face identity and face emotion processing. The main focus though will be on electrophysiological studies which have provided evidence for both high-level sparse encoding and also distributed population encoding as well as some differences in responses in left and right hemispheres. The effects of learning will be discussed together with view-dependent and view-independent and norm-based aspects of encoding as well as mental imagery. The roles of face-stimulus evoked changes in theta and gamma frequency activity will also be discussed and the use of neural network models and simulations to aid functional interpretation of neurophysiological data Introduction One of the long held assumptions in the field of face recognition research, namely that specialised processing of face cues was a facet of primate social evolution, was dispelled when we first published electrophysiological findings from sheep inferotemporal cortex reporting the presence of populations of face-sensitive neurons broadly similar to those found in monkeys (Kendrick and Baldwin 1987). From our subsequent detailed behavioural, neuroanatomical mapping and further electrophysiological studies in sheep (Tate et al., 2006) it has become clear that specialised face recognition systems in the brain are likely to have evolved more as a general facet of mammalian social evolution and are probably present in a number or ungulate and other mammalian species with complex social systems and well developed visual acuity. As such, neurophysiological and behavioural studies on sheep face recognition can be considered broadly relevant as a model for helping to understand similar, although undoubtedly more complex, processes in humans. Face recognition in sheep The first behavioral evidence for face recognition in sheep came from observations that maternal sheep found it difficult to recognise their lambs when the latter had their heads artificially colored (Alexander and Shillito-Walser, 1977). Subsequently, using various face discrimination paradigms it has been possible to show that sheep have a highly developed expertise. This was shown initially in a simple two-choice maze where sheep could immediately discriminate between face pictures of individuals with differential attraction (socially familiar vs unfamiliar sheep or sheep vs humans) in order to gain access to the individual whose face they had seen (Kendrick et al., 1995, 1996). Then, using food to reward accurate discrimination between individuals of similar attraction, it was shown both in a two choice maze, or with an