Feature-selective responses in macaque visual cortex follow eye movements during natural vision

• Published in: Nature neuroscience 2024-06, Vol.27 (6), p.1157-1166
• Main Authors: Xiao, Will, Sharma, Saloni, Kreiman, Gabriel, Livingstone, Margaret S.
• Format: Article
• Language: English
• Subjects: 631/378/116/2395; 631/378/2613/1875; 631/378/2613/2614; 631/378/3917; Animal Genetics and Genomics; Animals; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Computational neuroscience; Eye; Eye movements; Eye Movements - physiology; Female; Fixation, Ocular - physiology; Macaca mulatta; Male; Monkeys; Monkeys & apes; Neural networks; Neurobiology; Neurons; Neurons - physiology; Neurosciences; Photic Stimulation - methods; Receptive field; Retina; Saccades - physiology; Temporal lobe; Viewing; Vision; Vision, Ocular - physiology; Visual cortex; Visual Cortex - physiology; Visual Perception - physiology
• ISSN: 1097-6256; 1546-1726; 1546-1726
• DOI: 10.1038/s41593-024-01631-5

In natural vision, primates actively move their eyes several times per second via saccades. It remains unclear whether, during this active looking, visual neurons exhibit classical retinotopic properties, anticipate gaze shifts or mirror the stable quality of perception, especially in complex natural scenes. Here, we let 13 monkeys freely view thousands of natural images across 4.6 million fixations, recorded 883 h of neuronal responses in six areas spanning primary visual to anterior inferior temporal cortex and analyzed spatial, temporal and featural selectivity in these responses. Face neurons tracked their receptive field contents, indicated by category-selective responses. Self-consistency analysis showed that general feature-selective responses also followed eye movements and remained gaze-dependent over seconds of viewing the same image. Computational models of feature-selective responses located retinotopic receptive fields during free viewing. We found limited evidence for feature-selective predictive remapping and no viewing-history integration. Thus, ventral visual neurons represent the world in a predominantly eye-centered reference frame during natural vision. Xiao et al. show that, in monkeys freely viewing natural images, visual neurons from V1 to the inferior temporal cortex encode feature information in the gaze-centered space with limited predictive remapping and develop a neural network model to map the receptive fields.