Encoding of 3D Head Orienting Movements in the Primary Visual Cortex

• Published in: Neuron (Cambridge, Mass.) Mass.), 2020-11, Vol.108 (3), p.512-525.e4
• Main Authors: Guitchounts, Grigori, Masís, Javier, Wolff, Steffen B.E., Cox, David
• Format: Article
• Language: English
• Subjects: active sensing; Animals; corollary discharge; Cortex (motor); Eye movements; Female; Head; Head Movements - physiology; Light; movement; naturalistic behavior; Neural coding; Orientation behavior; Orientation, Spatial - physiology; Photic Stimulation; predictive coding; Proprioception - physiology; Rats; Rats, Long-Evans; Somatosensory cortex; Visual cortex; Visual Cortex - physiology; Visual stimuli
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2020.07.014

Animals actively sample the sensory world by generating complex patterns of movement that evolve in three dimensions. Whether or how such movements affect neuronal activity in sensory cortical areas remains largely unknown, because most experiments exploring movement-related modulation have been performed in head-fixed animals. Here, we show that 3D head-orienting movements (HOMs) modulate primary visual cortex (V1) activity in a direction-specific manner that also depends on light. We identify two overlapping populations of movement-direction-tuned neurons that support this modulation, one of which is direction tuned in the dark and the other in the light. Although overall movement enhanced V1 responses to visual stimulation, HOMs suppressed responses. We demonstrate that V1 receives a motor efference copy related to orientation from secondary motor cortex, which is involved in controlling HOMs. These results support predictive coding theories of brain function and reveal a pervasive role of 3D movement in shaping sensory cortical dynamics. [Display omitted] •Primary visual cortex (V1) encodes 3D head-orienting movements (HOMs)•V1 neurons are modulated by HOMs depending on light and are tuned to HOM direction•Responses to visual stimulation are suppressed during HOMs•HOM encoding depends on secondary motor cortex (M2) Guitchounts et al. find that the primary visual cortex (V1) of freely moving rats encodes 3D orienting movements of the head (HOMs). V1 is suppressed or enhanced by HOMs, depending on lighting condition, and individual neurons encode HOM direction. This encoding depends on secondary motor cortex (M2).