Abstract
Visual information is processed hierarchically along a ventral (‘what’) pathway that terminates with categorical representation of biologically relevant visual percepts (such as faces) in the mammalian extrastriate visual cortex. How birds solve face and object representation without a neocortex is a long-standing problem in evolutionary neuroscience, though multiple lines of evidence suggest that these abilities arise from circuitry fundamentally similar to the extrastriate visual cortex. The aim of the present experiment was to determine whether birds also exhibit a categorical representation of the avian face-region in four visual forebrain structures of the tectofugal visual pathway: entopallium (ENTO), mesopallium ventrolaterale (MVL), nidopallium frontolaterale (NFL), and area temporo-parieto-occipitalis (TPO). We performed electrophysiological recordings from the right and left hemispheres of 13 pigeons while they performed a Go/No-Go task that required them to discriminate between two sets of stimuli that included images of pigeon faces. No neurons fired selectively to only faces in either ENTO, NFL, MVL, or TPO. Birds’ predisposition to attend to the local-features of stimuli may influence the perception of faces as a global combination of features, and explain our observed absence of face-selective neurons. The implementation of naturalistic viewing paradigms in conjunction with electrophysiological and fMRI techniques has the potential to promote and uncover the global processing of visual objects to determine whether birds exhibit category-selective patches in the tectofugal visual forebrain.
Highlights
Birds derived their visual forebrain structures from an archosaur reptile roughly 320 million years ago (Jarvis et al, 2005)
The neuronal mechanisms by which visual categories are represented in the avian visual system is currently undetermined, but likely arises from circuitry that is homologous with associative cell-types found in the mammalian extrastriate visual cortex (Atoji and Karim, 2014; Briscoe et al, 2018)
All electrode tracks were within the borders of the targeted ENTO, nidopallium frontolaterale (NFL), mesopallium ventrolaterale (MVL), and TPO regions (Karten and Hodos, 1967; Stacho et al, 2016)
Summary
Birds derived their visual forebrain structures from an archosaur reptile (diapsid amniotes including living crocodilians and extinct dinosaurs) roughly 320 million years ago (Jarvis et al, 2005). The avian visual system exhibits a nuclear organisation that bears almost no resemblance to the six-layered mammalian neocortex, and is instead composed of densely clustered neuronal cell bodies (Reiner et al, 2004; Briscoe et al, 2018). Complex and view invariant representations of biologically relevant object categories, such as scenes (Kornblith et al, 2013), body parts (Pinsk et al, 2009), and faces (Tsao et al, 2003; Freiwald and Tsao, 2010) emerge in extrastriate cortex. Electrophysiological recordings from six functionally connected regions (known as ‘face-patches’) of macaque extrastriate cortex contain populations of neurons that respond with extreme selectively to faces (Tsao et al, 2003; Tsao et al, 2006; Moeller et al, 2017). The macaque ‘face-patch’ system generates a highly viewinvariant 3-D representation of facial identity
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