Dynamic light filtering over dermal opsin as a sensory feedback system in fish color change

• Published in: Nature communications Vol. 14; no. 1; pp. 4642 - 11
• Main Authors: Schweikert, Lorian E., Bagge, Laura E., Naughton, Lydia F., Bolin, Jacob R., Wheeler, Benjamin R., Grace, Michael S., Bracken-Grissom, Heather D., Johnsen, Sönke
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 22.08.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 14/19; 14/28; 38; 631/378/2613; 631/601/1737; 631/601/18; Animals; Chromatophores; Color; Color vision; Feedback; Humanities and Social Sciences; Lachnolaimus maximus; Morphology; multidisciplinary; Optics; Photoreception; Photoreceptors; Physiology; Pigments; Science; Science (multidisciplinary); Sensory evaluation; Sensory feedback; Skin; Skin preparations
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-40166-4

Dynamic color change has evolved multiple times, with a physiological basis that has been repeatedly linked to dermal photoreception via the study of excised skin preparations. Despite the widespread prevalence of dermal photoreception, both its physiology and its function in regulating color change remain poorly understood. By examining the morphology, physiology, and optics of dermal photoreception in hogfish ( Lachnolaimus maximus ), we describe a cellular mechanism in which chromatophore pigment activity (i.e., dispersion and aggregation) alters the transmitted light striking SWS1 receptors in the skin. When dispersed, chromatophore pigment selectively absorbs the short-wavelength light required to activate the skin’s SWS1 opsin, which we localized to a morphologically specialized population of putative dermal photoreceptors. As SWS1 is nested beneath chromatophores and thus subject to light changes from pigment activity, one possible function of dermal photoreception in hogfish is to monitor chromatophores to detect information about color change performance. This framework of sensory feedback provides insight into the significance of dermal photoreception among color-changing animals. Despite its prevalence, the function of dermal photoreception in color-changing animals remains poorly understood. Here, the authors describe an optical mechanism in hogfish skin, suggesting that one function is to obtain sensory feedback about color change performance.