Neuroendocrine control of the avian eyes

The nerve supplies in vertebrate eye originate from the ciliary and pterygopalatine parasympathetic ganglia, cervical sympathetic ganglia and sensory trigeminal axons. The sympathetic and parasympathetic pathways regulate ocular homeostasis. (Neuhuber and Schrödl, Reference NEUHUBER and SCHRÖDL2011). The preoptic area is a key site for the integration of sensory inputs and the initiation of motor outputs. Furthermore, prominent connections between the preoptic area and the periaqueductal grey matter form a node that is regulated by steroid hormones. This node receives sensory inputs and sends efferent projections to the brainstem and spinal cord that activate male sexual behaviours (Balla and Balthazart, Reference BALLA and BALTHAZART2004). In chicks, there is a neural crest-dependent signalling mechanism that is used to integrate different components of the eye, and it plays a general role for coordinating central and peripheral parts of the sensory nervous system (Grocott et al., Reference GROCOTT, JOHNSON, BAILEY and STREIT2011). Neural responses of the luminance and colour mechanisms direct accommodation and emmetropisation mechanisms to different focal planes. Therefore, it is likely that the set point of refraction and accommodation is dependent on the sensitivity of the eye to changes in spatial and temporal as well as colour and luminance contrast (Rucker, Reference RUCKER2013). The cells of chick embryo retina produce growth hormone, which acts as an autocrine/paracrine and anti-apoptotic factor in the regulation of programmed cell death during retinal development (Sanders et al., Reference SANDERS, LIN, PARKER and HARVEY2010).

Effects of light stimulus on the components of the eye

The cornea is the major refractive component of the eye and serves as a barrier to the external environment (Ritchey et al., Reference RITCHEY, CODE, ZELINKA, SCOTT and FISCHER2011). When chicks are exposed to constant light during growth, their cornea becomes flatter and lighter in weight, and their anterior segments become shallower than those of chicks exposed to cyclical periods of light and dark (Wahl et al., Reference WAHL, LI, TAKAGI and HOWLAND2011).

The choroid is a source of growth factors that can act on neighbouring tissues. Visual stimuli can cause changes in choroidal gene expression and choroid thickness. The choroid secretes scleral-growth regulators in response to visual stimuli. Choroidal retinaldehyde dehydrogenase-2 activity and retinoic acid synthesis modulate scleral remodelling (Summers, Reference SUMMERS2013). Many ocular processes show diurnal oscillations that optimize retinal function under the different conditions of ambient illumination, encountered over the course of the 24-hour light/dark cycle. Abolishing the diurnal cues by the use of constant darkness or constant light results in excessive ocular elongation, corneal flattening, and attendant refractive errors (Nickla, 2013). Peripheral defocus, higher-order aberrations and visual accommodation interact with pupil size to influence retinal image quality and possibly eye growth (Ostrin et al., Reference OSTRIN, LIU, CHOH and WILDSOET2011).

The lens cytosol is transparent as a result of short-range-order interactions between the proteins in spite of the presence of high levels of protein. At a cellular level, the programmed elimination of nuclei and other light-scattering organelles from cells located within the pupillary space contributes directly to tissue transparency (Bassnett et al., Reference BASSNETT, SHI and VRENSEN2011). The refractive power of a lens is determined largely by its surface curvatures and the refractive index of its medium. These properties can also be used to control the sharpness of focus and, hence, the image quality. One of the most effective ways of doing this is with a gradient index (Pierscionek and Regini, Reference PIERSCIONEK and REGINI2012). As the eye changes focus, the resulting alterations in cone contrast are associated with changes in colour and luminance. Changes in refraction are mainly due to alternations in eye length, with colour flicker producing much greater changes in eye length than luminance flick (Rucker and Wallman, Reference RUCKER and WALLMAN2012).

Roles of retinal photoreceptors in light perception of the eyes

Light of different wavelengths has varying stimulatory effects on the retina and can result in behavioural changes that may affect the growth and development of chickens (Lan et al., Reference LAN, LI, WANG, ZHAO, LIU and ZHU2013). Birds have ultra-violet-sensitive visual pigments with sensitivity maxima around either 360 – 373 nm (ultra-violent sensitive) or 402 – 426 nm (violet-sensitive). However, some birds with violet-sensitive pigments have unexpectedly low ultra-violet transmission of the ocular media, probably because of ultra-violet blocking lens pigmentation (Lind et al., Reference LIND, MITKUS, OLSSON and KELBER2014). Photostimulation of retinal photoreceptors, which are sensitive to green light, appears to inhibit reproductive activity in birds, whereas photostimulation of extra-retinal photoreceptors, which are sensitive to red light, accelerates it. This finding suggests that selective photostimulation of extra-retinal photostimulation, not retinal photostimulation, is key factor in the determination of successful reproduction of broiler breeder hens (Mobarkey et al., Reference MOBARKEY, AVITAL, HEIBLUM and ROZENBOIM2010).

The photochemistry of vision in all eyes employs an opsin and the isomerisation of a retinoid from the 11-cis to the all-trans configuration. The opsins, however, are associated with several different G proteins, initiating hyperpolarising and depolarising conductance changes at the photoreceptor membrane (Goldsmith, Reference GOLDSMITH2013). Absorption of a light particle by an opsin-pigment causes photo-isomerisation of its retinaldehyde chromophore. Restoration of light sensitivity to the resulting apo-opsin requires chemical re-isomerisation of the photobleached chromophore (Kaylor et al., Reference KAYLOR, YUAN, COOK, SARFARE, MAKSHANOFF, MIU, KIM, KIM, HABIB, ROYBAL, XU, NUSINOWITZ and TRAVIS2013). Furthermore, retinal ganglion cells expressing the photopigment melanopsin display intrinsic photosensitivity. The early expression onset of non-visual phototransduction molecules could confer premature photosensitivity to retinal ganglion cells, while the appearance of Opn4x expression in horizontal cells suggests the identification of a novel type of photosensitive cell in birds (Verra et al., Reference VERRA, CONTÍN, HICKS and GUIDO2011).

The thyroid hormone stimulates the maturation of photoreceptors in the avian retina by inhibiting the expression of lens-induced myopia domain transcription factors (Islet 2 and Lim 3) (Fischer et al., Reference FISCHER, BONGINI, BASTAKI and SHERWOOD2011). During retinal development, the cell-fate of photoreceptors is committed long before maturation, which entails the expression of opsins and functional transduction of light. Dopamine is one of the retinal neurotransmitters involved in the signalling cascade that controls eye growth by vision. Initially, reduced retinal dopamine levels were observed in eyes deprived of sharp vision by either diffusers (‘deprivation myopia’) or negative lenses (‘lens induced myopia’). Simulating high retinal dopamine levels by intra-vitreal application of a dopamine agonist can suppress the development of both deprivation myopia and lens induced myopia (Feldkaemper and Schaeffel, Reference FELDKAEMPER and SCHAEFFEL2013).

Functional inner retinal photoreceptors participate in the regulation of non-image-forming activities in non-mammalian vertebrates (Valdez et al., Reference VALDEZ, NIETO, GARBARINO-PICO, AVALLE, DÍAZ-FAJRELDINES, SCHURRER, CHENG and GUIDO2009). The retinal pigment epithelium constitutes a monolayer of cuboidal cells that interact apically with the interphotoreceptor matrix, outer segments of the photoreceptor cells and basally with the subjacent Bruch's membrane. This highly polarised structure is maintained by the cytoskeleton of individual cells and their interactions at the basolateral junctional complexes that stabilise this epithelial structure (Bonilha, Reference BONILHA2014). The close packing of vertebrate photoreceptors presents a challenge to the exchange of molecules between the outer segments, retinal pigmented epithelium, and Müller glia. An extracellular hyaluronic scaffold separates these cells, while soluble interphotoreceptor matrix proteins traffic visual cycle retinoids, fatty acids, and other molecules between them. In the interphotoreceptor matrix, retinoids and fatty acids are carried by interphotoreceptor retinoid-binding protein (Garlipp and Gonzalez-Fernandeza, Reference GARLIPP and GONZALEZ-FERNANDEZA2013).

Relationship between photoreceptors and colour vision of the avian eyes

Many invertebrate and vertebrate species have colour vision, that is, the ability to discriminate objects based on the wavelength of emitted light, independent of intensity. It requires at least two photoreceptor types with different spectral sensitivities and this process is often mediated by a mosaic made of several photoreceptor types (Rister and Desplan, Reference RISTER and DESPLAN2011). Attempts to understand the photoreceptor mechanisms mediating non-image-forming responses to light, such as photo-entrainment, have resulted in the discovery of a remarkable array of different photoreceptors and photopigment families, all of which appear to use a basic opsin/vitamin A-based photopigment biochemistry. In non-mammalian vertebrates, specialised photoreceptors are located within the pineal complex, deep brain and dermal melanophores (Peirson et al., Reference PEIRSON, HALFORD and FOSTER2009). There are two types of photoreceptors in birds: cones and rods. Cones are structures with robust and conical shape, having cell bodies arranged in a single row underneath the outer limiting membrane. Their inner and outer segments extend into the sub-retinal space towards the pigment epithelium, and are concentrated in foveal retina and have cell bodies layered in oblique columns under the outer limiting membrane. On the contrary, rods are slim rod-like in structure, which occupies the area between the larger cones in the sub-retinal space, stretching to the pigment epithelium cells. Rod cell bodies make up the rest of the outer nuclear layer below the cone cell bodies (Pearring et al., Reference PEARRING, SALINAS, BAKER and ARSHAVSKY2013).

Many types of cone receptors, sensitive to specific wave lengths, are involved in colour vision (Suzuki et al., Reference SUZUKI, BLECKERT, WILLIAMS, TAKECHI, KAWAMURA and WONG2013). The differences in the density and distribution of photoreceptors results in non-uniformity in the perception of colour vision across the retina. The overlapping of high density cone photoreceptors in retinal areas, with a high density of ganglion cells, increases the discrimination of the vision (Moore et al., Reference MOORE, BAUMHARDT, DOPPLER, RANDOLET, BLACKWELL, DEVAULT, LOEW and FERNÁNDEZ-JURICIC2012). Colour signals are expected to match visual sensitivities of intended receivers. The shifts from violet-sensitive (V-type) to ultraviolet-sensitive (U-type) vision in the avian species have been linked to high occurrence of colours with abundance of shortwave reflectance (ultraviolet/blue), owing to better perception of such colours by U-type vision (Delhey et al., Reference DELHEY, HALL, KINGMA and PETERS2012). Furthermore, four types of cone visual pigments and a single type of rod visual pigment exist (Sato et al., Reference SATO, YAMASHITA, IMAMOTO and SHICHIDA2012). The photoreceptors in cells of cones and rods of vertebrate retinas have visual pigments made up of photoreceptive proteins. These proteins are composed of an opsin protein moiety and a light-absorbing chromophore, 11-cis-retinal. Cone photoreceptors are arranged in geographically mosaic fashion in many vertebrate species. The mosaic arrangement of the photoreceptors is hypothesised to be maintained by differential cell-cell adhesion (Zou et al., Reference ZOU, WANG and WEI2012).

Birds are highly visual animals with five different cone photoreceptor subtypes, yet their photoreceptor patterns are not perfectly regular. By analysing the chicken cone photoreceptor system, consisting of five different cell types, using a variety of sensitive microstructural descriptors, the disordered photoreceptor patterns are ‘hyperuniform’ (exhibiting vanishing infinite-wavelength density fluctuations), a property that had been identified in a unique subset of physical systems, but had never been observed in any living organism (Jiao et al., Reference JIAO, LAU, HATZIKIROU, MEYER-HERMANN, CORBO and TORQUATO2014).

Photoperiodicity in birds

Circadian rhythms are endogenous 24-hour cycles that persist in the absence of external time cues. These rhythms provide an internal representation of day length and optimise physiology and behaviour to the varying demands of the solar cycle. These clocks require daily adjustment to local time, and the primary time cue (zeitgeber) used by most vertebrates is the daily change in the amount of environmental light (irradiance) at dawn and dusk, a process termed ‘photo entrainment’ (Peirson et al., Reference PEIRSON, HALFORD and FOSTER2009). In most species daily rhythms are synchronised by the photoperiodic cycle. They are generated by the circadian system, which is made up of a pacemaker, an entrainment pathway to this clock, and one or more output signals. In vertebrates, melatonin produced by the pineal organ is one of these outputs. The production of this time-keeping hormone is high at night and low during the day (Falcón et al., Reference FALCÓN, BESSEAU, FUENTÈS, SAUZET, MAGNANOU and BOEUF2009). The circadian clock is a fundamental property of living organisms and is involved in seasonal (photoperiodic) time measurement. Among vertebrates, birds have multiple circadian pacemakers in the eye, the pineal gland, and the suprachiasmatic nucleus, and have highly sophisticated photoperiodic mechanisms. However, because the removal of these circadian pacemakers fails to abolish the photoperiodic response, the existence of another ‘photoperiodic clock’ has been suggested (Ikegami et al., Reference IKEGAMI, KATOU, HIGASHI and YOSHIMURA2009). Annual changes in day length induce marked changes in reproductive function in temperate zone vertebrates. In many avian species, plasticity in hypothalamic gonadotropin-releasing hormone–1 expression rather than (or in addition to) its release governs changes in pituitary–gonadal activity (Stevenson et al., Reference STEVENSON, BERNARD, MCCARTHY and BALL2013).

Roles of melatonin and other hormones in lighting and photoperiodicity

The hormone melatonin is secreted primarily from the pineal gland, with highest levels occurring during the dark period of a circadian cycle. This hormone, through an action in the brain, appears to be involved in the regulation of various neural and endocrine processes that are cued by the daily change in photoperiod (Li et al., Reference LI, QING, ZHAO, XU, ZHAO and ZHU2011). Daily rhythms of melatonin in isolated pinealocytes and in intact pineal glands under in vivo conditions were demonstrated during the last third of embryonic development in chick embryos, with higher levels occurring during the dark than during the light phase (Zeman and Herichová, Reference ZEMAN and HERICHOVÁ2011). Circadian rhythm of melatonin biosynthesis of chickens is established by second day of post-embryonic life and it is dependent on season (Piesiewicz et al., Reference PIESIEWICZ, KEDZIERSKA, PODOBAS, ADAMSKA, ZUZEWICZ and MAJEWSKI2012). Melatonin is required for normal corneal growth in vivo, and together melatonin and retinoic acid, or the latter alone, affects the regulation of water content within the chick cornea, and melatonin affects corneal hydration in vitro (Wahl et al., Reference WAHL, LI, TAKAGI and HOWLAND2011). Furthermore, it plays a role in stimulating gonadotropin-inhibiting hormone (GnIH) peptide release from the hypothalamus in quail, thus inhibiting plasma LH concentrations and providing a mechanism by which changes in day length can influence reproduction in this species (Chowdhury et al., Reference CHOWDHURY, YAMAMOTO, UBUKA, BENTLEY, HATTORI and TSUTSUI2010; Reference CHOWDHURY, UBUKA and TSUTSUIB2013). The receptor for GnIH is the G protein-coupled receptor 147 (GPR147), which inhibits cAMP signalling. Cell bodies of GnIH neurones are located in the paraventricular nucleus in birds (Ubuka et al., Reference UBUKA, SON, TOBARI, NARIHIRO, BENTLEY, KRIEGSFELD and TSUTSUI2014). Besides, it has been demonstrated that melatonin decreases fearful responses in broiler chickens (Sinkalu and Ayo, Reference SINKALU and AYO2011), maintains thermal homeostasis and reduces erythrocyte osmotic fragility in layer hens (Sinkalu et al., Reference SINKALU, AYO, ABIMBOLA and IBRAHIM2014a) during the daytime period of the hot-dry season in the Northern Guinea Savannah zone of Nigeria.

The retinal pigment epithelial cells and the cone cells are intraocular sources of α-melanocyte-stimulating hormone (α-MSH) in the embryonic and postnatal life of the chicken (Teshigawara et al., Reference TESHIGAWARA, TAKAHASHI, BOSWELL, LI, TANAKA and TAKEUCHI2001). The presence and possible physiological roles of α-MSH in the peripheral tissues of birds have not been established yet. However, it is suggested that embryonic expression of α-MSH in the retinal pigment epithelial cells implies a possible role for the α-MSH in ocular development (Teshigawara et al., Reference TESHIGAWARA, TAKAHASHI, BOSWELL, LI, TANAKA and TAKEUCHI2001).

Use of light manipulation in poultry production

The use of lower lighting intensity may be beneficial to commercial poultry facilities that utilise low lighting environment to reduce hyperactivity, pecking damage and energy costs without physiological stress effects on broiler welfare (Olanrewaju et al., Reference OLANREWAJU, PURSWELL, COLLIER and BRANTON2011). Deep et al. (Reference DEEP, SCHWEAN-LARDNER, CROWE, FANCHER and CLASSEN2012) showed that exposure to light intensity of 1 Lux resulted in reduction of welfare of birds. Low light intensity may exert detrimental effect on egg production in the early laying phase, as well as influences the time allocated to different behaviours (O'connor et al., Reference O'CONNOR, PARKER, DAVEY, GRIST, OWEN, SZLADOVITS, DEMMERS, WATHES and ABEYESINGH2011). Light intensity manipulation is an important management tool affecting broiler behaviour and physiology. Low-contrast light intensity dampened behavioural rhythms and induced health adverse effects (Blatchford et al., Reference BLATCHFORD, ARCHER and MENCH2012). Artificially supplemented light at night time show that red and white lights increases eating, and, hence, weight gain (Senaratna et al., Reference SENARATNA, SAMARAKONE, MADUSANKA and GUNAWARDANE2011). Studies suggest that green and white lights have strong effects on immunity, especially at the last days of rearing, due to the proliferation of peripheral blood T lymphocytes. Exposing chicks to high illuminances, either sunlight or intense laboratory lights, retards the development of experimental myopia. Therefore, it is suggested that daily exposure to high light levels may have a protective effect (Ashby et al., Reference ASHBY, OHLENDORF and SCHAEFFEL2009).

Reddy et al. (Reference REDDY, DAVID, SELVARAJU, MONDAL and KIRAN2012) showed that in laying hens aged 72–78 week old high levels of gonadotropin releasing hormone-1 mRNA, luteinising hormone, estrogen-2β, and progesterone concentration induced an increased egg production, even later in the productive period, by modulating the wavelengths of light under normal husbandry conditions. It has also been shown that laying hens, reared under red light, mature earlier, and their egg production and egg shell thickness increased, but did not improve feed conversion rate (Min et al., Reference MIN, HOSSAN, NAZMA, JAE, HAN, HWAN, DONG, HYUN, HEE and OK2012). Zahoor et al. (Reference ZAHOOR, MIAN, AHMAD, NADEEM, REHMAN and AKRAM2011) found similar results in laying birds subjected to 16-hour light, 2-hour and 1-hour night-interruptions. Although pullet lighting regimen showed little effect on bone mineralisation at end of lay (Hester et al., Reference HESTER, WILSON, SETTAR, ARANGO and O'SULLIVAN2011), appropriate prelay short day exposure is required to fully photosensitise juvenile hens for photo-induced egg production, and this requires a development time beyond 16 week of age (Siopes, Reference SIOPES2010). Jatoi et al. (Reference JATOI, KHAN, SAHOTA, AKRAM, JAVED, JASPAL and KHAN2013) demonstrated that the highest body weight and egg production in laying quails was recorded under 8L:6D or 2L:8D lighting regimen, while higher feed intake was observed under treatment with 16L:8D. This finding may have been due to the fact that more light supplied to the birds increased feeding activity of the birds. Besides, the birds could see the feeds when exposed to light, and melatonin secretion may have been reduced during the increased light exposure, resulting in stress. Archana (Reference ARCHANA2012) showed that melatonin supplementation at 2.0 mg/kg feeds to laying hens improved the egg weight, egg volume, albumen and yolk volume, egg shell weight and thickness. This finding was supported by that of Sinkalu et al. (Reference SINKALU, AYO, ADELAIYE and HAMBOLU2014b), who demonstrated that continuous lighting regimen was stressful to broiler chickens not treated with melatonin, but melatonin administration ameliorated the adverse effects of the photo-stressful conditions in the birds. This finding demonstrated potential beneficial role of the antioxidant property of melatonin in improving broiler production.

Continuous lighting programmes induce high electrical energy consumption (Abreu et al., Reference ABREU, DE ABREU, COLDEBELLA, JAENISCH, DOS SANTOS FILHO and DE PAIVA2011). Amakiri et al. (Reference AMAKIRI, OWEN and ETOKEREN2011) demonstrated that it is wasteful for broiler farmers to incur additional cost of providing and/or extending the duration of light. In contrast with continuous lighting, intermittent lighting improved broiler chickens’ antioxidant status and non-specific immunity (Zheng et al., Reference ZHENG, MA, GU, YUAN, SHI, GUO and ZHAN2013). Gous and Cherry (Reference GOUS and CHERRY2004) suggested that a nutritional stimulus late in rearing is only necessary for satisfactory egg production in broiler breeders, if birds have not received a concurrent increment in photoperiod. Furthermore, seven-day-old male broiler chickens presented better feed conversion under light-emitting diode bulbs illumination than did males of the same age under compact fluorescent lamps (Mendes et al., Reference MENDES, PAIXÃO, RESTELATTO, MORELLO, DE MOURA and POSSENTI2013). Hence, the use of light-emitting diode in poultry housing is apparently, advantageous because of its energy efficiency and long life, compared to the conventional light sources. It has the additional benefit of its various colours and higher productivity (Parvin et al., Reference PARVIN, MUSHTAQ, KIM and CHOI2014). Monochromatic light is a potential light source that may provide a beneficial effect on growth performance (Kim et al., Reference KIM, PARVIN, MUSHTAQ, HWANGBO, KIM, NA, KIM, KANG, KIM, CHO, YANG and CHOI2013). Broiler chickens reared in yellow light house have been demonstrated to record a significant increase in total serum protein, while those in blue light house showed reduction in serum triglyceride, glucose and BUN concentrations (Firouzi et al., Reference FIROUZI, NAZARPAK, HABIBI, JALALI, NABIZADEH, REZAEE, ARDALI and MARZBAN2014).