Spatial modulation of dark versus bright stimulus in the mouse visual system

• Authors: Brice Williams, Georgia Institute of Technology; Joseph Del Rosario, Georgia Institute of Technology; Tomaso Muzzu, University College London; Kayla Peelman, Georgia Institute of Technology; Stefano Coletta, Georgia Institute of Technology; Edyta K Bichler, Georgia Institute of Technology; Anderson Speed, Georgia Institute of Technology; Lisa Meyer-Baese, Georgia Institute of Technology; Aman B Saleem, University College London; Bilal Haider, Emory University
• Journal Title: CURRENT BIOLOGY
• Volume: Volume 31, Number 18
• Publisher: CELL PRESS | 2021-09-27, Pages 4172-4179.e6
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1016/j.cub.2021.06.094
• Subjects: Engineering, Biomedical
• Keywords: Science & Technology; Life Sciences & Biomedicine; Biochemistry & Molecular Biology; Biology; Cell Biology; Life Sciences & Biomedicine - Other Topics; RECEPTIVE-FIELDS; CORTEX; POTENTIALS; RESPONSES; CIRCUITS; NEURONS; FASTER; LAYERS; SPACE; CELLS

Abstract

A fundamental task of the visual system is to respond to both increases and decreases of luminance with action potentials (ON and OFF responses1–4). OFF responses are stronger, faster, and more salient than ON responses in primary visual cortex (V1) of both cats5,6 and primates,7,8 but in ferrets9 and mice,10 ON responses can be stronger, weaker,11 or balanced12 in comparison to OFF responses. These discrepancies could arise from differences in species, experimental techniques, or stimulus properties, particularly retinotopic location in the visual field, as has been speculated;9 however, the role of retinotopy for ON/OFF dominance has not been systematically tested across multiple scales of neural activity within species. Here, we measured OFF versus ON responses across large portions of visual space with silicon probe and whole-cell patch-clamp recordings in mouse V1 and lateral geniculate nucleus (LGN). We found that OFF responses dominated in the central visual field, whereas ON and OFF responses were more balanced in the periphery. These findings were consistent across local field potential (LFP), spikes, and subthreshold membrane potential in V1, and were aligned with spatial biases in ON and OFF responses in LGN. Our findings reveal that retinotopy may provide a common organizing principle for spatial modulation of OFF versus ON processing in mammalian visual systems.