A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds

Abstract

It has been known for many decades that nonmammalian vertebrates detect light by deep brain photoreceptors that lie outside the retina and pineal organ to regulate seasonal cycle of reproduction. However, the identity of these photoreceptors has so far remained unclear. Here we report that Opsin 5 is a deep brain photoreceptive molecule in the quail brain. Expression analysis of members of the opsin superfamily identified as Opsin 5 (OPN5; also known as Gpr136, Neuropsin, PGR12, and TMEM13) mRNA in the paraventricular organ (PVO), an area long believed to be capable of phototransduction. Immunohistochemistry identified Opsin 5 in neurons that contact the cerebrospinal fluid in the PVO, as well as fibers extending to the external zone of the median eminence adjacent to the pars tuberalis of the pituitary gland, which translates photoperiodic information into neuroendocrine responses. Heterologous expression of Opsin 5 in Xenopus oocytes resulted in light-dependent activation of membrane currents, the action spectrum of which showed peak sensitivity (λ max ) at ∼420 nm. We also found that short-wavelength light, i.e., between UV-B and blue light, induced photoperiodic responses in eye-patched, pinealectomized quail. Thus, Opsin 5 appears to be one of the deep brain photoreceptive molecules that regulates seasonal reproduction in birds.circadian rhythms | Japanese quail | photoperiodism | paraventricular organ | cerebrospinal fluid-contacting neuron

The saccus vasculosus of fish is a sensor of seasonal changes in day length

“…3a), whereas the CSF-contacting neurons are bipolar neurons with a knob-like structure; their morphology resembles that of photoreceptor cells in the developing retina 18 . In a previous study, we demonstrated that OPN5-positive CSFcontacting neurons in the quail hypothalamus are a type of deep-brain photoreceptors that mediate the photoperiodic response 10 . Therefore, we predicted that opsins would be expressed in CSF-contacting neurons in the SV.…”

“…As the CSF-contacting neuron is the deep-brain photoreceptor in quail 10 , it is reasonable to speculate that some of these opsins may be expressed in CSF-contacting neurons, to act as another type of photoreceptor in the SV. This possibility remains to be examined in a future study.…”

“…In birds, by contrast, melatonin has little effect on photoperiodic response of gonads 8 . Furthermore, neither eyes nor the pineal organ, another photoreceptive organ in non-mammalian vertebrates, are necessary for the photoperiodic response in birds 9 ; instead, light received by the deep-brain photoreceptors induces expression of TSH in the PT 10 . Most fish living outside the tropics also exhibit a photoperiodic response 11 , and involvement of thyroid hormone in the regulation of seasonal reproduction has been described extensively 12 .…”

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

“…The response is found to be tuned to short-wavelength (390-410 nm) UV illumination, and focal illumination experiments reveal that a confined region of caudal diencephalon is required to generate the response. Moreover, immunostaining for OPN5, a known UV-sensitive opsin (8,9), and cryptochrome 1, a blue-light sensor found in Drosophila (20,21), reveals cells in this region of the tadpole diencephalon that express proteins with an appropriate spectral sensitivity. Together, these results suggest that Xenopus larvae are equipped with short wavelength-sensitive neurons deep within the brain that directly link environmental luminance to motor output and may underlie a simple light avoidance response and/or potentially overlay classical circadian systems.…”

“…In addition, it was demonstrated that lesions to the diencephalon removed this response, implying that the periventricular tissue of the brain was directly light-sensitive. Since then, deep-brain photoreception, specifically in the hypothalamus, has been studied extensively in relation to its role in gonadal induction in birds (4)(5)(6)(7)(8)(9).…”