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A spinal opsin controls early neural activity and drives a behavioral light response.

ABSTRACT: Nonvisual detection of light by the vertebrate hypothalamus, pineal, and retina is known to govern seasonal and circadian behaviors. However, the expression of opsins in multiple other brain structures suggests a more expansive repertoire for light regulation of physiology, behavior, and development. Translucent zebrafish embryos express extraretinal opsins early on, at a time when spontaneous activity in the developing CNS plays a role in neuronal maturation and circuit formation. Though the presence of extraretinal opsins is well documented, the function of direct photoreception by the CNS remains largely unknown. Here, we show that early activity in the zebrafish spinal central pattern generator (CPG) and the earliest locomotory behavior are dramatically inhibited by physiological levels of environmental light. We find that the photosensitivity of this circuit is conferred by vertebrate ancient long opsin A (VALopA), which we show to be a G?(i)-coupled receptor that is expressed in the neurons of the spinal network. Sustained photoactivation of VALopA not only suppresses spontaneous activity but also alters the maturation of time-locked correlated network patterns. These results uncover a novel role for nonvisual opsins and a mechanism for environmental regulation of spontaneous motor behavior and neural activity in a circuit previously thought to be governed only by intrinsic developmental programs.

SUBMITTER: Friedmann D

PROVIDER: S-EPMC4286461 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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A spinal opsin controls early neural activity and drives a behavioral light response.

Friedmann Drew D Hoagland Adam A Berlin Shai S Isacoff Ehud Y EY

Current biology : CB 20141204 1

Nonvisual detection of light by the vertebrate hypothalamus, pineal, and retina is known to govern seasonal and circadian behaviors. However, the expression of opsins in multiple other brain structures suggests a more expansive repertoire for light regulation of physiology, behavior, and development. Translucent zebrafish embryos express extraretinal opsins early on, at a time when spontaneous activity in the developing CNS plays a role in neuronal maturation and circuit formation. Though the pr ...[more]

PMID: 25484291

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Project description:BackgroundAnimals living in well-lit environments utilize optical stimuli for detecting visual information, regulating the homeostatic pacemaker, and controlling patterns of body pigmentation. In contrast, many subterranean animal species without optical stimuli have evolved regressed binocular eyes and body pigmentation. Interestingly, some fossorial and cave-dwelling animals with regressed eyes still respond to light. These light-dependent responses may be simply evolutionary residuals or they may be adaptive, where negative phototaxis provides avoidance of predator-rich surface environments. However, the relationship between these non-ocular light responses and the underlying light-sensing Opsin proteins has not been fully elucidated.MethodsTo highlight the potential functions of opsins in a blind subterranean animal, we used the Mexican cave tetra to investigate opsin gene expression in the eyes and several brain regions of both surface and cave-dwelling adults. We performed database surveys, expression analyses by quantitative reverse transcription PCR (RT-qPCR), and light-dependent locomotor activity analysis using pinealectomized fish, one of the high-opsin expressing organs of cavefish.ResultsBased on conservative criteria, we identified 33 opsin genes in the cavefish genome. Surveys of available RNAseq data found 26 of these expressed in the surface fish eye as compared to 24 expressed in cavefish extraocular tissues, 20 of which were expressed in the brain. RT-qPCR of 26 opsins in surface and cavefish eye and brain tissues showed the highest opsin-expressing tissue in cavefish was the pineal organ, which expressed exo-rhodopsin at 72.7% of the expression levels in surface fish pineal. However, a pinealectomy resulted in no change to the light-dependent locomotor activity in juvenile cavefish and surface fish. Therefore, we conclude that, after 20,000 or more years of evolution in darkness, cavefish light-dependent basal activity is regulated by a non-pineal extraocular organ.

Dataset Information

A spinal opsin controls early neural activity and drives a behavioral light response.

Publications

A spinal opsin controls early neural activity and drives a behavioral light response.

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