Single-unit activity during natural vision: diversity, consistency, and spatial sensitivity among AF face patch neurons

• Published in: The Journal of neuroscience Vol. 35; no. 14; pp. 5537 - 5548
• Main Authors: McMahon, David B T, Russ, Brian E, Elnaiem, Heba D, Kurnikova, Anastasia I, Leopold, David A
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 08.04.2015
• Subjects: Action Potentials - physiology; Animals; Attention - physiology; Evoked Potentials, Visual - physiology; Female; Image Processing, Computer-Assisted; Macaca mulatta; Magnetic Resonance Imaging; Male; Neurons - physiology; Oxygen - blood; Pattern Recognition, Visual - physiology; Principal Component Analysis; Space Perception - physiology; Time Factors; Vision, Ocular - physiology; Visual Cortex - blood supply; Visual Cortex - cytology; movies; fMRI; macaque; single units; eigenneurons; natural vision
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.3825-14.2015

Several visual areas within the STS of the macaque brain respond strongly to faces and other biological stimuli. Determining the principles that govern neural responses in this region has proven challenging, due in part to the inherently complex stimulus domain of dynamic biological stimuli that are not captured by an easily parameterized stimulus set. Here we investigated neural responses in one fMRI-defined face patch in the anterior fundus (AF) of the STS while macaques freely view complex videos rich with natural social content. Longitudinal single-unit recordings allowed for the accumulation of each neuron's responses to repeated video presentations across sessions. We found that individual neurons, while diverse in their response patterns, were consistently and deterministically driven by the video content. We used principal component analysis to compute a family of eigenneurons, which summarized 24% of the shared population activity in the first two components. We found that the most prominent component of AF activity reflected an interaction between visible body region and scene layout. Close-up shots of faces elicited the strongest neural responses, whereas far away shots of faces or close-up shots of hindquarters elicited weak or inhibitory responses. Sensitivity to the apparent proximity of faces was also observed in gamma band local field potential. This category-selective sensitivity to spatial scale, together with the known exchange of anatomical projections of this area with regions involved in visuospatial analysis, suggests that the AF face patch may be specialized in aspects of face perception that pertain to the layout of a social scene.