Deep Brain Photoreceptors Control Light-Seeking Behavior in Zebrafish Larvae

Abstract

Summary Most vertebrates process visual information using elaborately structured photosensory tissues including the eyes and pineal. However there is strong evidence that other tissues can detect and respond to photic stimuli [1, 2, 3]. Many reports suggest that photosensitive elements exist within the brain itself and influence physiology and behavior, however a long standing puzzle has been the identity of the neurons and photoreceptor molecules involved [4, 5]. We tested whether light cues influence behavior in zebrafish larvae through deep brain photosensors. We found that larvae lacking eyes and pineal perform a simple light-seeking behavior triggered by loss of illumination (`dark photokinesis'). Neuroanatomical considerations prompted us to test orthopedia (otpa) deficient fish which showed a profound reduction in dark photokinesis. Using targeted genetic ablations, we narrowed the photosensitive region to neurons in the preoptic area. Neurons in this region express several photoreceptive molecules, but expression of the melanopsin opn4a is selectively lost in otpa mutants, suggesting that opn4a mediates dark photokinesis. Our findings shed light on the identity and function of deep brain photoreceptors and suggest that otpa specifies an ancient population of sensory neurons that mediate behavioral responses to light.

Deep-brain photoreception links luminance detection to motor output in Xenopus frog tadpoles

“…In the zebrafish hypothalamus the nonretinal opsin, melanopsin (OPN4), is coexpressed with tyrosine hydroxylase (TH) within A-11-type dopaminergic neurons and, although their function is unknown, it is presumed they may be important for light-mediated locomotor responses (16). We found no evidence that OPN5 was located within dopaminergic neurons (Fig.…”

“…In zebrafish, the photoreceptors underlying dark photokinesis have been localized to the anterior preoptic area, and they transduce light via the photopigment melanopsin (16). The photosensitivity we report in Xenopus is not mediated by the equivalent region of the brain because the preoptic area has been removed in these light-sensitive preparations.…”

“…The photosensitivity we report in Xenopus is not mediated by the equivalent region of the brain because the preoptic area has been removed in these light-sensitive preparations. However, melanopsin was also found more caudally in zebrafish, in neurons of the PT (16), an area that is present in the light-sensitive Xenopus preparations. This finding is particularly relevant because the cells in question were A-11-type dopaminergic neurons that comprise a diencephalospinal population implicated in motor control (28).…”

“…The fish will swim away from a bright light and generally prefer dark conditions, but in a dark environment will swim toward a localized region of light. Although the eyes are required for proper orientation toward a light stimulus, a general increase in motor activity upon loss of illumination, termed dark photokinesis, persists in enucleated fish (16). Using genetic manipulations, Fernandes et al (16) were able to narrow the photosensitive region to a population of melanopsin-positive neurons of the anterior preoptic area.…”

“…Although the eyes are required for proper orientation toward a light stimulus, a general increase in motor activity upon loss of illumination, termed dark photokinesis, persists in enucleated fish (16). Using genetic manipulations, Fernandes et al (16) were able to narrow the photosensitive region to a population of melanopsin-positive neurons of the anterior preoptic area. Another light-driven but nonvisual, nonpineal motor behavior displayed by larval zebrafish is the photomotor response [PMR (17)].…”