Encoding of 3D Head Orienting Movements in Primary Visual Cortex

Abstract

Animals actively sample from the sensory world by generating complex patterns of movement that evolve in three dimensions. At least some of these movements have been shown to influence neural codes in sensory areas. For example, in primary visual cortex (V1), locomotion-related neural activity influences sensory gain, encodes running speed, and predicts the direction of visual flow. As most experiments exploring movement-related modulation of V1 have been performed in head-fixed animals, it remains unclear whether or how the naturalistic movements used to interact with sensory stimulilike head orienting-influence visual processing. Here we show that 3D head orienting movements modulate V1 neuronal activity in a direction-specific manner that also depends on the presence or absence of light. We identify two largely independent 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. Finally, we demonstrate that V1 gains access to a motor efference copy related to orientation from secondary motor cortex, which has been shown to control head orienting movements. These results suggest a mechanism through which sensory signals generated by purposeful movement can be distinguished from those arising in the outside world, and reveal a pervasive role of 3D movement in shaping sensory cortical dynamics.

Dynamical processing of orientation precision in the primary visual cortex

“…Although the temporal nature of this code has been explored through temporal generalization (28), an intrinsic limit to our investigation is the lack of large-scale simultaneous recordings. Previous publications have reported population decoding by merging neural activity across electrodes or experiments (46, 47), which we validated in our data (Supplementary Figure 6).…”

How Cortical Circuits Implement Cortical Computations: Mouse Visual Cortex as a Model

“…Incorporating movement information can enable an organism to more accurately reconstruct the visual scene by correcting for self-motion, as well as by enabling the extraction of additional features such as depth through motion parallax (Leopold & Park 2020, Parker et al 2020. Consistent with these roles, neurons in rat V1 encode a representation of the three-dimensional rotation of the head in space (Guitchounts et al 2020). Likewise, the speed and direction of movement play predictive roles in processing visual inputs in V1, resulting in mismatch signals when the visual input does not correspond to that expected during locomotion (Leinweber et al 2017).…”

A compact spatial map in V2 visual cortex

“…During navigation, spatial context modulates neuronal responses in the visual cortex (Flossmann and Rochefort, 2020; Nau et al, 2018; Saleem, 2020) and visual thalamus (Hok et al, 2018). Head movement, orientation, direction and locomotion signals were detected in the rodent V1(Bouvier et al, 2020; Guitchounts et al, 2020a; Guitchounts et al, 2020b; Meyer et al, 2018; Saleem et al, 2013; Velez-Fort et al, 2018). Additionally, coherent coding of spatial signals was found in the rodent primary visual cortex (V1) and hippocampal CA1 subfield (Fournier et al, 2020; Haggerty and Ji, 2015; Ji and Wilson, 2007).…”