Localization and characterization of val‐opsin isoform‐expressing cells in the brain of adult zebrafish

Abstract

In addition to vision, light information is used to regulate a range of animal physiology. Such nonimage-forming functions of light are mediated by nonvisual photoreceptors expressed in distinct neurons in the retina and the brain in most vertebrates. A nonvisual photoreceptor vertebrate ancient long opsin (VAL-opsin) possesses two functional isoforms in the zebrafish, encoded by valopa and valopb, which has received little attention. To delineate the neurochemical identities of valop cells and to test for colocalization of the valop isoforms, we used in situ hybridization to characterize the expression of the valop genes along with that of neurotransmitters and a neuropeptide known to be present at the sites of valop expression. Double labeling showed that the thalamic valop population coexpresses valopa and valopb. All the thalamic valop cells overlapped with a GABAergic cell mass that continues from the anterior nucleus to the intercalated thalamic nucleus. A novel valopa cell population found in the superior raphe was serotonergic in nature. A valopb cell population in the Edinger-Westphal nucleus was identified as containing thyrotropin-releasing hormone. Valopb cells localized in the hindbrain intermediate reticular formation were noncholinergic in nature (nonmotorneurons). Thus, the presence of valop cell populations in different brain regions with coexpression of neurotransmitters and neuropeptides and the colocalization of valop isoforms in the thalamic cell population indicate regulatory and functional complexity of VAL-opsin in the brain of the zebrafish.

Organization of alpha‐transducin immunoreactive system in the brain and retina of larval and young adult Sea Lamprey (Petromyzon marinus), and their relationship with other neural systems

“…Non‐mammalian vertebrates possess a wide range of intrinsically photoreceptive sites expressing members of the non‐visual opsin family (see Hankins, Davies, & Foster, ). ISH studies in the brain of zebrafish and other teleosts have revealed different neuronal populations that express opsins (Philp et al, ; Matos‐Cruz et al, ; Fischer et al, ; Nakane et al, ; Eilertsen et al, ; Hang, Kitahashi, & Parhar, ; Sato et al, ). Some of the Opn5 (neuropsin)‐expressing forebrain populations of medaka and zebrafish (Sato et al, ) are located in regions similar to those containing the post‐optic/hypothalamic opsin and/or transducin‐expressing CSF‐c neuronal populations of lampreys (García‐Fernández & Foster, ; García‐Fernández et al, ; present results).…”

Brain area‐specific diurnal and photic regulation of val‐opsinA and val‐opsinB genes in the zebrafish

“…), and found different neurotransmitters (GABA, serotonin) or neuropeptide (thyrotropin‐releasing hormone) in each valop cell group in the adult brain (Hang et al . ). The majority of valop cells (co‐expressing both isoforms) are located in the thalamus and minority cell groups (with single valop isoform) in the midbrain and hindbrain.…”

Deep Brain Photoreceptor (val-opsin) Gene Knockout Using CRISPR/Cas Affects Chorion Formation and Embryonic Hatching in the Zebrafish

“…In the zebrafish, the VAL-opsin isoforms are expressed in both the eyes and the brain [10, 11, 15], and the VAL-opsin photoreceptors in the eyes and the brain are thought to play distinct roles in zebrafish physiology [16]. Furthermore, VAL-opsinA and VAL-opsinB photoreceptors are expected to have distinct functions in the eyes [11].…”

“…In the current study, F0 valopa and valopb mutants exhibited a similar parental-effect phenotype in their eggs and resultant embryos. Our previous work determined the co-expression of valopa and valopb in the thalamic valop cell group within the brain, which may play a GABA-dependent modulatory role in light-dependent physiology [15, 16]. There is evidence of seasonal variation in the levels of GABA-synthesizing enzymes in the brain and GABA control on pituitary gonadotropin release in fish species [53–57].…”

“…Two isoforms of zebrafish VAL-opsin, encoded by the val-opsinA ( valopa ) and val-opsinB ( valopb ) genes [11], exist and might have separate functions. Indeed, our recent studies concluded that VAL-opsin isoforms are involved in different neurochemical systems in multiple brain regions and mediate the control of time- and light-dependent physiology and behaviours in adult zebrafish [15, 16]. However, no reverse genetic studies have been conducted to study the functions of deep brain opsins including VAL-opsin in non-mammalian models.…”