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

• Published in: Current biology 2021-09, Vol.31 (18), p.4172-4179.e6
• Main Authors: Williams, Brice, Del Rosario, Joseph, Muzzu, Tomaso, Peelman, Kayla, Coletta, Stefano, Bichler, Edyta K., Speed, Anderson, Meyer-Baese, Lisa, Saleem, Aman B., Haider, Bilal
• Format: Article
• Language: English
• Subjects: LFP; luminance; membrane potential; retinotopy; single units; visual cortex
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.06.094

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. [Display omitted] •Dark stimuli in the central visual field drive strong OFF responses in awake mice•Dark and bright stimuli in the periphery drive more balanced OFF and ON responses•LFP and membrane potential responses in binocular V1 show clear OFF dominance•ON/OFF responses in V1 and lateral geniculate (LGN) show retinotopic alignment Visual system neurons respond to both bright and dark stimuli (ON and OFF responses); it remains unclear which of these dominate mammalian vision. Williams et al. measure these responses across visual cortex and thalamus in awake mice and find that stimuli in the central visual field drive stronger OFF responses than stimuli in the far periphery.