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Melanopsin photoreception plays a vital role in irradiance detection for non-image forming responses to light. However, little is known about the involvement of melanopsin in emotional processing of luminance. When confronted with a gradient in light, organisms exhibit spatial movements relative to this stimulus. In rodents, behavioural light aversion (BLA) is a well-documented but poorly understood phenomenon during which animals attribute salience to light and remove themselves from it. Here, using genetically modified mice and an open field behavioural paradigm, we investigate the role of melanopsin in BLA. While wildtype (WT), melanopsin knockout (Opn4(-/-)) and rd/rd cl (melanopsin only (MO)) mice all exhibit BLA, our novel methodology reveals that isolated melanopsin photoreception produces a slow, potentiating response to light. In order to control for the involvement of pupillary constriction in BLA we eliminated this variable with topical atropine application. This manipulation enhanced BLA in WT and MO mice, but most remarkably, revealed light aversion in triple knockout (TKO) mice, lacking three elements deemed essential for conventional photoreception (Opn4(-/-) Gnat1(-/-) Cnga3(-/-)). Using a number of complementary strategies, we determined this response to be generated at the level of the retina. Our findings have significant implications for the understanding of how melanopsin signalling may modulate aversive responses to light in mice and humans. In addition, we also reveal a clear potential for light perception in TKO mice.

Original publication

DOI

10.1371/journal.pone.0015009

Type

Journal article

Journal

PLoS One

Publication Date

29/11/2010

Volume

5

Keywords

Animals, Atropine, Avoidance Learning, Channelrhodopsins, Cyclic Nucleotide-Gated Cation Channels, Electroretinography, GTP-Binding Protein alpha Subunits, Humans, Immunohistochemistry, Kinetics, Light, Mice, Mice, 129 Strain, Mice, Inbred C57BL, Mice, Knockout, Motor Activity, Parasympatholytics, Proto-Oncogene Proteins c-fos, Regression Analysis, Retina, Rod Opsins, Transducin, Visual Cortex