Exploring avian deep-brain photoreceptors and their role in activating the neuroendocrine regulation of gonadal development

Abstract

A large number of mammalian, avian, and other vertebrate species are photoperiodic and thereby display a defined time of year when their reproductive system is activated due to an ability to sense seasonal changes in photoperiod. Several reviews have addressed photoperiodism in birds including its proposed mechanisms, regulation of key annual cycle events, and relevance to productivity and fitness of avian species Nicholls et al., 1988;Kuenzel, 1993;Foster et al., 1994;Wilson, 1997;Dawson et al., 2001;Sharp, 2005;Ono et al., 2009;Ubuka et al., 2013). The purpose of this paper is to focus on one aspect of the phenomenon, particularly its sensory component. Decades ago it was proposed that vertebrates possess a photo-neuroendocrine system (PNES) composed of 2 components including (1) the photoperiodic axis (receptors and groups of neurons detecting light or changes in photoperiods, and (2) the traditional hypothalamo-pituitary-gonadal (HPG) axis (Scharrer, 1964). Scharrer's first component, the sensory system, will be addressed herein. A neural pathway is required to detect light information from the environment, integrate it and in some manner connect with the classical HPG axis to regulate reproductive function at the appropri- ABSTRACT In the eyes of mammals, specialized photoreceptors called intrinsically photosensitive retinal ganglion cells (ipRGC) have been identified that sense photoperiodic or daylight exposure, providing them over time with seasonal information. Detectors of photoperiods are critical in vertebrates, particularly for timing the onset of reproduction each year. In birds, the eyes do not appear to monitor photoperiodic information; rather, neurons within at least 4 different brain structures have been proposed to function in this capacity. Specialized neurons, called deep brain photoreceptors (DBP), have been found in the septum and 3 hypothalamic areas. Within each of the 4 brain loci, one or more of 3 unique photopigments, including melanopsin, neuropsin, and vertebrate ancient opsin, have been identified. An experiment was designed to characterize electrophysiological responses of neurons proposed to be avian DBP following light stimulation. A second study used immature chicks raised under shortday photoperiods and transferred to long day lengths. Gene expression of photopigments was then determined in 3 septal-hypothalamic regions. Preliminary electrophysiological data obtained from patch-clamping neurons in brain slices have shown that bipolar neurons in the lateral septal organ responded to photostimulation comparable with mammalian ipRGC, particularly by showing depolarization and a delayed, slow response to directed light stimulation. Utilizing real-time reversetranscription PCR, it was found that all 3 photopigments showed significantly increased gene expression in the septal-hypothalamic regions in chicks on the third day after being transferred to long-day photoperiods. Each dissected region contained structures previously proposed to have DBP. The highly significant increased ge...

Impact of different light colors in behavior, welfare parameters and growth performance of Fayoumi broiler chickens strain

“…Domestic fowl differs from human in spectral sensitivity which illustrates the importance to identify the optimal light environment for health, behavior, welfare and production of broiler chickens. They are sensitive to ultraviolet, blue, green and red on the light spectrum (Prescott and Wathes, 1999) through retinal and deep brain photoreceptors (Kuenzel et al, 2015). Moreover, they also have 3 advanced light receptors within the brain that play a foremost role in the biological and physiological functions (Bertolucci and Foa, 2004;Wyse and Hazlerigg, 2009).…”

Connecting spectral radiometry of anthropogenic light sources to the visual ecology of organisms

“…To determine how the artificial light sources would stimulate myriad visual systems, we calculated quantal catch for each photoreceptor of the selected organisms: an averaged ultraviolet sensitive Passeriformes visual system (UV/VIS) (Hart, 2001;Endler & Mielke, 2005;Maia et al, 2013), an average nonultraviolet sensitive avian visual system (V/VIS) (Hart, 2001(Hart, , 2002Maia et al, 2013), a human (Dartnall, Bowmaker & Mollon, 1983), a Wolf (Jacobs et al, 1993), a hawkmoth (Schlecht, 1979;Briscoe & Chittka, 2001), and we also included the deep brain photoreceptors of birds (Kuenzel et al, 2014). Specifically, birds have tetrachromatic color vision meaning they have four different classes of photoreceptors that are involved in opponent processing enabling a bird to perceive different colors Endler & Mielke, 2005;Ghim & Hodos, 2006;Hart & Hunt, 2007).…”

“…The double cones are an intermediary between the tetrachromatic color vision, which require bright conditions and rods which are only activated in very dim light conditions. Birds also have photoreceptors located within the brain that detect photons from the environment that are transmitted through the bird's diaphanous skull (Wyse & Hazlerigg, 2009;Kuenzel et al, 2014). There are at least four deep brain photoreceptors: neuropsin, melanopsin, pinopsin and vertebrate ancient opsin (Max et al, 1995;Halford et al, 2009;Wyse & Hazlerigg, 2009;Kuenzel et al, 2014).…”

“…Organisms are chronically exposed to artificial lighting, which affects foraging, communication, circadian rhythms, endocrinology, predator-prey interactions, reproduction and other biological functions (Longcore, 2010; Dominoni et al, 2013;Br€ uning et al, 2015). Ultimately, these changes in animal behavior, physiology and ecology from artificial light at night are due to organismal reception of anthropogenically produced light (Kuenzel, Kang & Zhou, 2014;Alaasam et al, 2018). Millions of different species of organisms have evolved the ability to detect light for visual tasks and as cues for circadian rhythms and phenology, thus altering natural light conditions has grave ecological consequences (Cronin et al, 2014;Garc ıa-Fern andez et al, 2015;Davies & Smyth, 2017;Gaston et al, 2017).…”

“…In addition to the varied color vision of many animals, animals also have non-visual photoreceptors with different opsins that use light as a cue for biological functions, such as circadian rhythms, reproductive timing and sleep (Hattar et al, 2002;Halford et al, 2009;Gaston et al, 2017). These non-visual opsins in photoreceptors in vertebrates (referred to as deep brain photoreceptors) include melanopsin, neuropsin, pinopsin and vertebrate ancient opsin (Kuenzel et al, 2014;Dominoni, 2015). Melanopsin regulates circadian rhythms in vertebrates (Ruby et al, 2002).…”