Photosexual Response Research Articles

Seasonal reproductive state determines gene expression in the hypothalamus of a latitudinal migratory songbird during the spring and autumn migration

We investigated gonadal effects on hypothalamic transcription of genes in sham-operated and castrated redheaded buntings photostimulated into spring and autumn migratory states. RNA-Seq results showed testes-dependent differences between spring and autumn migratory states. In particular, differentially expressed genes enriched G-protein-coupled receptor and calcium-ion signaling pathways during spring and autumn states, respectively. qPCR assay showed attenuated gabra5, ttr, thra and thrb expressions, suggesting reduced GABA and thyroid hormone effects on photo-sexual response in spring. In spring castrates, reduced npy, tac1 and nrcam and increased ank3 expression suggested testicular effects on the appetite, prolactin release and neuronal functions, whereas in autumn castrates, reduced rasgrp1, grm5 and grin1, and increased mras expression suggested testicular effects on the ras, G-protein and glutamate signaling pathways. Castration-induced reciprocal switching of pomc and pdyn expressions suggested effects on the overall homeostasis in both seasons. These results demonstrate transcriptome-wide changes, with season-dependent roles of testes in songbird migration.

Specific neural phase relation of serotonin and dopamine modulate the testicular activity in Japanese quail.

Specific phase relation of serotonin and dopamine modulate the hypothalamo-hypophyseal-gonadal axis as well as photosexual responses in Japanese quail, but the effect of these specific phase relations on testicular activity and steroidogenesis is not yet been investigated. We hypothesized that temporal phase relation induced alteration in local testicular gonadotropin-releasing hormone (GnRH)-Gonadotropin-inhibitory hormone (GnIH) and their receptor system may modulate the testicular activity and steroidogenesis through local (paracrine and autocrine) action. To validate this hypothesis, we have checked the alterations in the expression of gonadotropin-releasing hormone receptor (GnRH-R), gonadotropin-inhibitory hormone receptor (GnIH-R) messenger RNA (mRNA), growth hormone receptor (GH-R), proliferating cell nuclear antigen (PCNA), cell communication and gap junctional proteins (14-3-3 and connexin-43 [Cnx-43]), steroidogenic factor-1 (SF-1), steroidogenic acute regulatory(StAR) protein, steroidogenic enzyme (3β-hydroxysteroid dehydrogenase [3β-HSD]) in testis as well as androgen receptor (AR) in testis and epididymis of control, 8-, and 12-hr quail. Experimental findings clearly indicate the increased expression of GnIH-R mRNA and suppression of GnRH-R, GH-R, PCNA, 14-3-3, Cnx-43, SF-1, StAR, 3β-HSD in testis as well as AR in testis and epididymis in 8-hr quail, while 12-hr quail exhibited the opposite results that is significantly decreased expression of GnIH-R mRNA and increased expression of GnRH-R, GH-R, PCNA, 14-3-3, Cnx-43, SF-1, StAR, 3β-HSD in testis as well as AR in testis and epididymis. The significantly increased intratesticular testosterone has been observed in the 12-hr quail while, 8-hr quail showed opposite result. Hence, it can be concluded that 12-hr quail showed significantly increased testicular activity and steroidogenesis while opposite pattern was observed in 8-hr quail.

Simulated photoperiod influences testicular activity in quail via modulating local GnRHR-GnIHR, GH-R, Cnx-43 and 14-3-3

The hypothalamo-hypophyseal-gonadal axis mediated differential photosexual responses in quail kept under different simulated photoperiodic conditions have been studied in details. Local testicular GnRH-GnIH and their receptor system has been hypothesized to be modulated in quail showing different photo-sexual responses and thus influence the testicular activity and steroidogenesis through local (paracrine and autocrine) action. To validate this hypothesis, we studied the expression of gonadotropin releasing hormone receptor (GnRH-R), gonadotropin inhibiting hormone receptor (GnIH-R) mRNA, growth hormone receptor (GH-R), proliferating cell nuclear antigen (PCNA), 14-3-3, Connexin-43 (Cnx-43), steroidogenic factor-1 (SF-1), Steroidogenic Acute Regulatory protein (StAR), steroidogenic enzyme (3β HSD) in testis as well as androgen receptor (AR) in testis and epididymis of photosensitive (PS), scotorefractory (SR), photorefractory (PR) and scotosensitive (SS) quail. Experimental findings clearly indicate the increased expression of GnIH-R mRNA and suppression of GnRH-R, GH-R, PCNA, 14-3-3, Connexin-43, SF-1, StAR, 3β HSD in testis as well as AR in testis and epididymis of PR and SS quail, while PS and SR quail exhibited the opposite results i.e., significantly decreased expression of GnIH-R mRNA and increased expression of GnRH-R, GH-R, PCNA, 14-3-3, Cnx-43, SF-1, StAR, 3β HSD in testis as well as AR in testis and epididymis. The significantly increased intra-testicular testosterone has been observed in the PS and SR quail while, PR and SS quail showed opposite results. Hence, we conclude that PS and SR quail showed significantly increased testicular activity and steroidogenesis while opposite pattern was observed in PR and SS quail.

Testicular atrophy and reproductive quiescence in photorefractory and scotosensitive quail: Involvement of hypothalamic deep brain photoreceptors and GnRH-GnIH system

Birds time their daily and seasonal activities in synchronization with circadian and annual periodicities in the environment, which is mainly provided by changes in photoperiod/day length conditions. Photoperiod appears to act at the level of eye, pineal and encephalic/deep brain photoperception and thus entrain the hypothalamic clock as well as reproductive circuitry in different avian species. In this article our focus of study is to elucidate out the underlying molecular mechanism of modulation of the hypothalamic reproductive circuitry following the photoperception through the hypothalamic photoreceptor cells and the subsequent alteration in the reproductive responses in quail, kept under different simulated photoperiodic conditions. Present study investigated the different simulated photoperiodic conditions induced hypothalamic DBP-GnRH-GnIH system mediated translation of photoperiodic information and subsequent exhibition of differential photosexual responses (scoto-/photo-sensitivity and refractoriness) in Japanese quail, Coturnix coturnix japonica. Paired testes weight and paired testicular volume increased 15.9 and 22.6-fold respectively in scotorefractory quail compare to that of scotosensitive phase and 12.8 and 24.3-fold in photosensitive quail compare to that of photorefractory phase. The pineal/eye melatonin (through melatonin receptor subtype Mel1cR) and hypothalamic deep brain photoreceptor (DBPs) cells directly modulate the hypothalamic GnRH-I/II and GnIH system and thus exhibit testicular stimulation or regression in response to different photoperiodic conditions (PS, PR, SS and SR). The hypothalamic alteration of DBP(s) and GnRH-GnIH system thus may induce the testicular stimulation in PS and SR quail and testicular regression in SS and PR quail.

Enhanced GABAergic inhibition in the premammillary nucleus of photorefractory turkey hens via GABAA receptor upregulation

The premammillary nucleus (PMM) of the turkey mediobasal hypothalamus, where dopamine-melatonin (DA-Mel) neurons are localized, is a site for photoreception and photoperiodic time measurement, which is essential for the initiation of avian reproductive seasonality. In addition, this area could also be responsible for the onset and maintenance of photorefractoriness at the end of the breeding season due to the enhanced inhibitory effect of γ-aminobutyric acid (GABA). GABA is an inhibitory neurotransmitter in the central nervous system which interferes with the photosexual response in the turkey, a seasonally breeding bird. Here, we further characterized the GABAA receptor subunits in the PMM DA-Mel neurons related to reproductive seasonality and the onset of photorefractoriness. GABAA receptor subunits and GABA synthesis enzymes in the PMM of photosensitive and photorefractory turkey hens were identified using real-time qRT-PCR. The upregulation of GABAA receptor α1-3, β2-3, γ1-3, ρ1-3, δ, and θ mRNA expression were observed in the PMM of photorefractory birds when compared to those of photosensitive ones while there is no change observed in the GABA synthesis enzymes, glutamate decarboxylase 1 and 2. Those upregulated GABAA receptor subunits were further examined using immunohistochemical staining and they appeared to be co-localized within the PMM DA-Mel neurons. The upregulation of GABAA receptor subunits observed in the PMM of photorefractory birds coincides with a lack of responsiveness to a light stimulus provided during the photosensitive phase. This is supported by the absence of c-fos induction and TH upregulation in the PMM and a subsequence inhibition of c-fos and GnRH-I expression in the nucleus commissurae pallii. The augmented GABAA receptor subunits expression may mediate an enhancement of inhibitory GABAergic neurotransmission and the subsequent interference with the photosexual response. This could contribute to the state of photorefractoriness and the termination of breeding activities in the turkey, a temperate zone bird.

Interaction of specific temporal phase relations of circadian neural oscillations and long term photoperiodic responses in Japanese quail, Coturnix coturnix japonica

Specific temporal phase relations of neural oscillations are reported to regulate gonadal activity in many avian species but their interaction with photo-sexual response are still unclear. Hence in the present study, 3week old Japanese quail maintained in short days (experiment 1) received normal saline (SD control) or serotonin precursor 5-HTP and dopamine precursor l-DOPA injections at the interval of 12h (SD 12-h) for 13days. At 37week of age, one subgroup of SD 12-h received these drugs at the interval of 8-h (SD 12-h+8-h). In the second experiment, 3week old quail were injected with 5-HTP and l-DOPA 8h apart (LD 8-h) and then maintained under long days. At the age of 37weeks, one subgroup of these LD quail was retreated with 5-HTP and l-DOPA at the interval of 8h (LD 8-h+8-h). Cloacal gland volume was monitored weekly up to 45weeks of age in both experiments and other reproductive parameters were monitored at 23 and 45week of age.These results indicate that 12-h phase relation of neurotransmitter precursors not only initiates early onset of scotorefractoriness i.e., full development of gonad even under short-day length but maintains it continuously (a long lasting effect) unlike control and the 8-h relation dissipates it, making the quail scotosensitive. On the other hand, the 8-h phase relation suppresses the gonado-stimulatory effect of long days but this effect is transitory. Thus the 12-h phase relation is gonado-stimulatory under short day conditions and the 8-h relation is gonado-inhibitory even under long days, inducing scotorefractoriness and photorefractoriness, respectively, it is suggested that effects of specific temporal phase relation of circadian neural oscillations similar to photoperiodic effects, are not only mediated by HPG axis but may also modulate the classical photoperiodic responses of Japanese quail.

Temporary exposure of prepubertal, somatically-mature broiler breeder females to stimulatory photoperiods

1. Individually-caged Ross 308 broiler breeders were transferred temporarily at 147 d from 8 to 14-h photoperiods and back to 8 h at 5-d intervals from 5 to 25 d and at 32 d. Control birds were maintained on 8 h or transferred permanently to 14 h. 2. Five long days had minimal effect on age at first egg, between 10 and 25 long days progressively accelerated sexual development, and maximum advance was achieved by 32 long days. However, a model involving the ogive of a normal distribution with a mean of 14 long days and an SD of 5.3 indicated that 28 long days would be sufficient to maximise sexual development. 3. The similarity of this model for broiler breeders with one previously produced for egg-type pullets suggested a common physiological mechanism for photosexual responses to two opposing changes in photoperiod.

Model to predict age at sexual maturity in broiler breeders given a single increment in photoperiod

1. Data from 9 experiments in which broiler breeder pullets had been photostimulated at two or more ages were integrated to produce a model to predict age at 50% egg production following a single increase in photoperiod during rearing. 2. It was clear that the photosexual response in broiler breeders was strongly influenced by the feed allowance and hence the rate of prepubertal growth. Regressions for birds given either a constant photoperiod or a single increase indicated that mean age at 50% lay advances by 2 d for every 100-g increase in body weight at 20 weeks. 3. The general response of broiler breeders was similar to that previously reported for egg-type pullets, but with important changes in the ages at which the birds progressed from one physiological state to the next, depending on body weight. 4. Broiler breeders, unlike modern egg-type pullets, exhibit juvenile photorefractoriness and, depending on their body weight, require up to 20 weeks to dissipate this (faster growth allows quicker dissipation). As a consequence, a group of birds grown to a typical weight of 2·1 kg at 20 weeks do not start to be photoresponsive until about 10 weeks and are not uniformly responsive until 19 or 20 weeks. A transfer to a stimulatory photoperiod before a bird has dissipated photorefractoriness causes a delay of about 3 weeks in its sexual development, and this results in a bimodal distribution of ages at maturity when a flock is photostimulated between 10 and 20 weeks. 5. Once photosensitive, the response of broiler breeders to an increment in photoperiod is between 0·50 and 0·65 of that observed in ISA Brown egg-type pullets. However, a flock of broiler breeders with typical feed restriction starts to mature spontaneously under the influence of the initial photoperiod from about 25 weeks. 6. There is a difference of only 1 to 3 d in age at 50% egg production between a flock transferred to 11 or 12 h followed by further increases to 15 or 16 h and one increased abruptly to one of these photoperiods, and so this model can be used to predict maturity in a commercial flock of birds even though they are likely to be given a stepped, rather than a single, increase in photoperiod.

Nitric oxide modulates gonadal and adrenal function in Japanese quail Coturnix coturnix japonica

Nitric oxide (NO) a gaseous neurotransmitter is reported to play an important role in controlling the release of luteinizing hormone releasing hormone (LHRH) in mammalian system. But its role has not been investigated in birds, where photoperiod plays an important role in regulating gonadal development. To investigate the effect of NO on gonadal and adrenal function of Japanese quail, in the first experiment, 3-weeks-old sexually immature quail received NO donor sodium nitroprusside (SNP, 5 mg/100 g body weight) orally or nitric oxide synthase (NOS) inhibitor N-nitro l-arginine methyl ester (L-NAME, 25 μg/100 g body weight) intraperitoneally for 13 days in continuous condition of light (LL). Thereafter treated quail along with their respective controls were shifted to long day length (LD 16:8) for 21 days when the study was terminated. Results indicate that SNP treatment stimulated and L-NAME suppressed body weight, cloacal gland volume (an androgen dependent sex accessory organ), testes (gonado-somatic index, spermatogenesis), epididymis (histology) and adrenal (weight, histology, cortico-medullary ratio) function as well as total nitrite and nitrate concentration in plasma, hypothalamus and testes. In the second experiment, two groups of 3-weeks-old birds were maintained in short day length (LD 6:18) or long day length (LD 16:8) for 5 weeks to induce gonadal suppression and stimulation, respectively. Thereafter birds of both the photoperiod were divided into two subgroups, the short day quail receiving normal saline (SD Con) or SNP (SD + SNP) while long day quail received normal saline (LD Con) or L-NAME (LD + L-NAME) for 13 days and were maintained in their respective photoperiods, until the termination of study (21 days post treatment period). SNP stimulated all the parameters even in short day condition and L-NAME suppressed in long day quail compared to their respective controls. These findings indicate positive control of NO on the gonad and adrenal function of Japanese quail which exhibits parallel adrenal–gonad relationship. Further, NO donor induces long day effects while NOS inhibitor mimics short day effects. It is concluded that NO may not only regulate hypothalamo–hypophyseal–gonadal and -adrenal axis of Japanese quail but may also modulate its photosexual responses.

Light-induced reduction of cytoplasmic free calcium in neurons proposed to be encephalic photoreceptors in chick brain

A population of cerebrospinal fluid-contacting neurons (CSFcn) in the lateral septal organ (LSO) may serve as encephalic photoreceptors (EPRs) functioning to signal the onset of seasonal reproductive development in birds. Previous studies on CSFcn in the LSO have focused on identification of retinal protein components in fixed brain tissue. In order to understand better the mechanisms underlying the light-induced photosexual response in birds, a physiological characterization is required. In this study, changes of intracellular free calcium concentration ([Ca 2+] i) were monitored during light stimulation of CSFcn in the LSO in live brain slices from embryonic chicks. Using the fluorescent calcium indicator fluo-4, a reduced [Ca 2+] i within CSFcn was recorded in response to photostimulation, which is consistent with what has been demonstrated in rods and cones following illumination. Results support the hypothesis that CSFcn in the LSO function as EPRs in the avian brain.

Constant photoperiods and sexual maturity in broiler breeder pullets

1. Broiler breeder pullets were maintained on 10-, 11-, 12-, 13-, 14- or 16-h photoperiods to determine the effect of constant photoperiods on sexual development in broiler breeders. The birds were fed to achieve a 2100 g body weight at approximately 17 or 20 weeks to see if the photosexual response was modified by rate of growth. 2. In both body weight groups, pullets maintained on 10 h were the first to reach sexual maturity (50 eggs/100 bird-d), and these and the 11-h pullets matured significantly earlier than any of the other photoperiod groups. Pullets maintained on 13 or 14 h matured latest, at about 3 weeks after the 10-h pullets, though both were only marginally later than the 12- or 16-h birds. These differences in maturation probably reflect the different rates at which photorefractoriness is dissipated in broiler breeders reared on photoperiods that vary in their degree of stimulatory competence. 3. There were no significant interactions among the photoperiods and the ages at 2100 g; faster-growing birds consistently matured about 10 d earlier than conventionally grown pullets.

Thyroid involvement in the relative photorefractoriness of Japanese quail, Coturnix coturnix japonica

AbstractThyroid involvement in the photosexual response was examined in photosensitive and relative photorefractory Japanese quail. Surgical thyroidectomy was carried out in gonadally regressed adult males held for several months on natural daylengths of 13.5–14.5 h. These birds were considered relative photorefractory (birds that are gonadally regressed at daylengths, 12–15 h, and initially stimulatory for gonadal growth in photosensitive quail). Following thyroidectomy and sham‐operation (controls), one‐half of each group were exposed for 30 days to light:dark (LD) 16:8 and then transferred to LD 13.5:10.5 for another 30 days. The remaining operated quail were exposed for the first 30 days to LD 8:16 and then transferred to LD 13.5:10.5 for another 30 days. In quail examined after the first 30 days, the left testis sizes were greatly increased in both thyroidectomized and control birds held on LD 16:8 but completely regressed in both groups held on LD 8:16. The photosexual responses are characteristic for both photosensitive and relative photorefractory quail held on such daylengths. After the second 30 days, the testes were strongly stimulated in both thyroidectomized and control quail that were transferred from LD 8:16 (first 30 days) to LD 13.5:10.5 (second 30 days). Apparently, photosensitivity had been reestablished during the first 30 days on short daylengths. In quail transferred from LD 16:8 (first 30 days) to LD 13.5:10.5 (second 30 days), the testis sizes were reduced in control birds indicating a relative photorefractory response to this intermediate daylength. However, the testis continued to grow in the thyroidectomized quail transferred from LD 16:8 to LD 13.5:10.5. The results indicate that the thyroid is important in the maintenance of relative photorefractoriness in Japanese quail.

Effects of photoperiod and temperature on ovarian activity in the Indian murrel, Channa (Ophiocephalus) punctatus (Bloch)

Channa punctatus (Bloch) is a seasonal breeder and spawns during the monsoon season. Ovarian regression occurs at a time when day length begins to shorten and temperature reaches a seasonal minimum, while the ovarian recrudescence coincides with the increase in day length and temperature. The close relationship between increasing day length and temperature suggests that these two factors are in some way involved in inducing gonadal recrudescence. Responses of the ovary to various combinations of photoperiod and temperature were studied during the postspawning and preparatory periods. Temperatures of 25 °C and above, regardless of photoperiod, were more favorable for the formation of yolky oocytes and ovarian development occurred as a function of warm temperature even under conditions of continuous darkness or continuous light. These studies have revealed that ovarian recrudescence, which normally occurs during the prespawning period, can be advanced by photothermal manipulations. It was concluded that photoperiod may be responsible for timing the seasonal reproductive activity; nevertheless, the rate of photosexual response is temperature dependent.

Participation of the eyes in the photosexual response of Japanese quail (Coturnix coturnix japonica).

Participation of the eyes in the photosexual response of Japanese quail (Coturnix coturnix japonica).

Participation of the Eyes in the Photostimulation of Chickens

This study examined the participation of the eyes in the photosexual response of chickens to incandescent and fluorescent light. Intact and blinded female chickens were exposed to short photoperiods (8L:16D) of incandescent and fluorescent light and the age at first egg and rate of egg production were determined. Incandescent light was inhibitory to the age at first egg and the early rate of egg production. Blinding prevented this response. It was concluded that the eye is not essential to the photosexual reponse of chickens but that it may modify the response to light in certain conditions.

The effects of blinding, pinealectomy and exposure to constant dark conditions on gonadal activity in the female goldfish, Carassius auratus

The effects of pinealectomy, blinding, and exposure to constant darkness were examined in female goldfish during different seasons. Neither blinding nor pinealectomy under short or decreasing photoperiod conditions, nor exposure to constant darkness had an effect on ovarian activity in goldfish during fall and winter. In spring, constant darkness has an inhibitory effect on ovarian activity. Pinealectomy under increasing photoperiod conditions partially inhibits reproductive activity, but not to the extent of constant darkness. Blinding, under the same regime also inhibited to some extent the ovarian response to increasing photoperiod. Our data suggest that retinal pathways and the pineal organ are involved in the photosexual response to increasing day lengths.

Ontogeny of the photosexual response in intact and castrated coturnix

This study examined the posthatch development of the photosexual response in intact and castrated coturnix. Two criteria were used to determine the onset of the effects of light: (1) the ability to distinguish between long and short photoperiods; and (2) the first increase in serum LH concentration. The results indicated that the onset of the photosexual reflex occurred between 3 and 4 weeks of age in females and between 17 and 21 days of age in males. The immature testes was shown to be involved in the developmental process of the photosexual reflex.

Lack of an effect of melatonin treatment via silastic capsules on photic-induced gonadal growth and the photorefractory condition in white-throated sparrows

The administration of melatonin via intraperitoneally placed Silastic capsules in white-throated sparrows failed to alter either photic-induced gonadal growth in females or the photorefractory condition in males. These results indicate that melatonin does not have a direct effect upon the avian photosexual response.

Photoreception in the photosexual response of quail. II. Effects of intensity and wavelength.

Photoreception in the photosexual response of quail. II. Effects of intensity and wavelength.

Photoreception in the photosexual response of quail. I. Site of photoreceptor.

ARTICLESPhotoreception in the photosexual response of quail. I. Site of photoreceptorT Oishi, and JK LauberT Oishi, and JK LauberPublished Online:01 Jul 1973https://doi.org/10.1152/ajplegacy.1973.225.1.155MoreSectionsPDF (1 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation More from this issue > Volume 225Issue 1July 1973Pages 155-158 Copyright & PermissionsCopyright © 1973 by American Physiological Societyhttps://doi.org/10.1152/ajplegacy.1973.225.1.155PubMed4714396History Published online 1 July 1973 Published in print 1 July 1973 Metrics