Exorhodopsin and melanopsin systems in the pineal complex and brain at early developmental stages of Atlantic halibut (Hippoglossus hippoglossus)

• Published in: Journal of comparative neurology (1911) 2014-12, Vol.522 (18), p.4003-4022
• Main Authors: Eilertsen, Mariann, Drivenes, Øyvind, Edvardsen, Rolf B., Bradley, Clarrisa A., Ebbesson, Lars O.E., Helvik, Jon Vidar
• Format: Article
• Language: English
• Subjects: Animals; Brain - growth & development; Brain - metabolism; Cloning, Molecular; Exorh; Fish Proteins - genetics; Fish Proteins - metabolism; Flounder - growth & development; Flounder - metabolism; Hippoglossus hippoglossus; Immunohistochemistry; In Situ Hybridization; Larva; larvae; Microscopy, Fluorescence; nonvisual opsin; Opn4; Photomicrography; photoreception; Pineal Gland - growth & development; Pineal Gland - metabolism; retina; Retina - growth & development; Retina - metabolism; Rhodopsin - genetics; Rhodopsin - metabolism; Rod Opsins - genetics; Rod Opsins - metabolism; RRID:AB_2336059; RRID:AB_2336060; RRID:AB_514497; RRID:AB_572263; RRID:AB_609894; RRID:AB_840257; RRID:nif-0000-02873; RRID:nif-0000-30609; RRID:nlx_153932; RRID:nlx_153933; RRID:nlx_156838; RRID:OMICS_00999; Sequence Homology; Teleostei
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23652

ABSTRACT The complexity of the nonvisual photoreception systems in teleosts has just started to be appreciated, with colocalization of multiple photoreceptor types with unresolved functions. Here we describe an intricate expression pattern of melanopsins in early life stages of the marine flat fish Atlantic halibut (Hippoglossus hippoglossus), a period when the unpigmented brain is directly exposed to environmental photons. We show a refined and extensive expression of melanopsins in the halibut brain already at the time of hatching, long before the eyes are functional. We detect melanopsin in the habenula, suprachiasmatic nucleus, dorsal thalamus, and lateral tubular nucleus of first feeding larvae, suggesting conserved functions of the melanopsins in marine teleosts. The complex expression of melanopsins already at larval stages indicates the importance of nonvisual photoreception early in development. Most strikingly, we detect expression of both exorhodopsin and melanopsin in the pineal complex of halibut larvae. Double‐fluorescence labeling showed that two clusters of melanopsin‐positive cells are located lateral to the central rosette of exorhodopsin‐positive cells. The localization of different photopigments in the pineal complex suggests that two parallel photoreceptor systems may be active. Furthermore, the dispersed melanopsin‐positive cells in the spinal cord of halibut larvae at the time of hatching may be primary sensory cells or interneurons representing the first example of dispersed high‐order photoreceptor cells. The appearance of nonvisual opsins early in the development of halibut provides an alternative model for studying the evolution and functional significance of nonvisual opsins. J. Comp. Neurol. 522:4003–4022, 2014. © 2014 Wiley Periodicals, Inc. The authors describe an advanced nonvisual system in Atlantic halibut, prior to the development of functional eyes, with melanopsin‐expressing cells in several brain regions and in spinal cord. In the pineal complex, melanopsin‐positive cells are found lateral and adjacent to the central rosette of exorhodopsin photoreceptors.