Melanopsin-Mediated Low Spatial Frequency Vision in Mice

Breakthroughs in Understanding Natural Behaviour and its Neural Underpinnings (University of Manchester, UK) (2024) Proc Physiol Soc 61, C03

Oral Communications: Melanopsin-Mediated Low Spatial Frequency Vision in Mice

Qian Huang1, Frank Martial1, Riccardo Storchi1, Robert Lucas1,

1Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine & Health, The University of Manchester MANCHESTER United Kingdom, 2Division of Neuroscience and Experimental Psychology, School of Biological Sciences, Faculty of Biology, Medicine & Health, The University of Manchester MANCHESTER United Kingdom,

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Keywords: low spatial frequency; preference choices; elevation range

Background: Behavioural and electrophysiological studies of pattern vision in mice typically address responses to high spatiotemporal frequency stimuli, but natural scenes contain patterns over a wide spatial frequency range. Coarse patterns contain information about important features of the local environment and yet we know little about how they are detected or how they impact mouse behaviour.

Aims: To establish behavioural and electrophysiological protocols for studying low-frequency vision in mice and to employ them to determine the contribution of the inner retinal photopigment melanopsin to this sensory modality.

Methods

We constructed a lighting arena capable of generating and quantifying low spatial frequency light patterns. This lighting arena consisted of two compartments, where the spatial distribution of light could be quantitatively controlled in each compartment. The light distribution across a -180° to 180° elevation range was quantified using the ELF method developed by Nilsson & Smolka (2021). Mice were placed into the lighting arena and we quantified time spent in each compartment as an indicator of preference. We used mice lacking cone (Cnga3-/-) or melanopsin (Opn4-/-) phototransduction and receptor silent substitution methods to separate the contribution of cone and melanopsin photoreceptors to pattern preference. Additionally, neural activity in the lateral geniculate nucleus of freely moving mice was recorded under these low-frequency spatial patterns.

Results

Our lighting arena is capable of generating various low-frequency spatial patterns, which we used in a series of behavioural trials. We found that these low-frequency spatial patterns could be detected and influence mouse choice at least as much as overall scene brightness. Local radiance around the horizon (-20° to 20°) primarily influenced mice’s preference choices. Mice preferred to spend time in the compartment where the horizon was darker. This preference was retained in Cnga3-/- but disrupted in Opn4-/- mice. Correspondingly, in silent substitution experiments, visually intact mice specifically preferred horizons and grounds darker for melanopsin, suggesting that melanopsin plays a primary role in detecting low-frequency spatial patterns. Electrophysiological recordings revealed increased firing rates and altered power spectra in response to low-frequency patterns, compared to brightness-matched uniform light. Further analysis of the electrophysiological data is ongoing.

Significance

Our findings demonstrate that mouse exploratory preferences are modulated by low-frequency patterns and especially by light intensity around the horizon. The detection of low-frequency spatial patterns appears to be mediated by melanopsin's sampling function.



Where applicable, experiments conform with Society ethical requirements.

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