Dissecting a role for melanopsin in behavioural light aversion reveals a response independent of conventional photoreception

• Published in: PloS one Vol. 5; no. 11; p. e15009
• Main Authors: Semo, Ma'ayan, Gias, Carlos, Ahmado, Ahmad, Sugano, Eriko, Allen, Annette E, Lawrence, Jean M, Tomita, Hiroshi, Coffey, Peter J, Vugler, Anthony A
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 29-11-2010; Public Library of Science (PLoS)
• Subjects: Animal cognition; Animals; Atropine; Atropine - pharmacology; Aversion; Avoidance Learning - drug effects; Avoidance Learning - radiation effects; Biology; Brain research; Channelrhodopsins; Cyclic Nucleotide-Gated Cation Channels - genetics; Cyclic Nucleotide-Gated Cation Channels - physiology; Electroretinography; Genetic modification; Genetically modified organisms; GTP-Binding Protein alpha Subunits - genetics; GTP-Binding Protein alpha Subunits - physiology; House mouse; Humans; Image detection; Immunohistochemistry; Interdisciplinary aspects; Irradiance; Kinetics; Light; Melanopsin; Mice; Mice, 129 Strain; Mice, Inbred C57BL; Mice, Knockout; Migraine; Motor Activity - drug effects; Motor Activity - radiation effects; Parasympatholytics - pharmacology; Photoreception; Physiology; Proto-Oncogene Proteins c-fos - metabolism; Regression Analysis; Retina; Retina - metabolism; Rod Opsins - genetics; Rod Opsins - physiology; Rodents; Signaling; Social and Behavioral Sciences; Spatial discrimination; Studies; Transducin - genetics; Transducin - physiology; Trends; Visual Cortex - metabolism; Visual Cortex - radiation effects
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0015009

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.