Photoreceptive oscillators within neurons of the premammillary nucleus (PMM) and seasonal reproduction in temperate zone birds

Kosonsiriluk, Sunantha; Mauro, Laura J.; Chaiworakul, Voravasa; Chaiseha, Yupaporn; Halawani, Mohamed E. El

doi:10.1016/j.ygcen.2013.02.015

Cited by 28 publications

(20 citation statements)

References 49 publications

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“…To date, how photoperiodic signals are communicated from both retinal photoreceptors and deep encephalic photoreceptors within the mediobasal hypothalamus to the avian ovary is unclear (51,52). Seasonal and daily photoperiodic signals serve to phase rhythms of ovarian activity.…”

Section: Mechanisms That Regulate Circadian Rhythmicity In Avian Ovarmentioning

confidence: 99%

The avian ovary and follicle development: some comparative and practical insights

Johnson¹

2014

Turk J Vet Anim Sci

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This review focuses on recent research related to the avian ovary and, in particular, cellular mechanisms mediating embryonic growth of the ovary, postembryonic follicular development, and the process of follicular selection. Attention is drawn to a variety of fundamental, yet unresolved, aspects of ovarian function, several of which are uniquely related to avian reproductive strategies. Some notable differences in ovarian function between birds and the most closely related extant group, the crocodilians, are illustrated. Moreover, because the sauropsid (reptilian and avian) and synapsid (mammalian) lineages diverged shortly after the emergence of amniotes some 340 million years ago, consideration is given to both derived and convergent characteristics of ovarian function in avian species versus those in eutherian mammals. Two examples of divergent characteristics are the differences in sex-determining mechanisms between birds and mammals and the requirement for progesterone synthesized within the follicular granulosa as a requirement for ovulation in virtually all species of birds, compared to the site of synthesis and role for estradiol in mammals. As an example of a convergent process, both birds and select mammals (e.g., humans, cattle, and horses) typically ovulate a single egg per reproductive cycle, yet the processes associated with follicular selection occur via unique mechanisms. Finally, reference is made to several practical outcomes from studies of the avian ovary, including applications within the poultry industry and use of the domestic hen ovary as a model for human ovarian cancer.

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Section: Mechanisms That Regulate Circadian Rhythmicity In Avian Ovarmentioning

confidence: 99%

The avian ovary and follicle development: some comparative and practical insights

Johnson¹

2014

Turk J Vet Anim Sci

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“…While considerable attention has been focused on defining the photoperiod-induced initiation of avian reproduction, the mechanisms underlying the onset of photorefractoriness remain hidden [5,6,19,20,21,22,23,24]. Considering the ability of the PMM to receive and interpret the light stimulus [10], we speculate that the failure of the photoperiodic entrainment in this nucleus may lead to the onset of photorefractoriness.…”

Section: Introductionmentioning

confidence: 97%

“…Unlike mammals, light information is received directly by the putative photoreceptive unit that resides within the avian basal hypothalamus, and is then integrated with the circadian clock to regulate reproductive seasonality [6,7]. Attempts to isolate the deep brain photoreceptor and the locale for photoperiodic time measurement responsible for regulating the avian reproductive system have been ongoing for several decades [6,8,9,10]. Several studies have focused on the mediobasal hypothalamus (MBH) [11,12], but a complete description of the neuronal circuitry that regulates the parameters of a breeding season is still lacking.…”

Section: Introductionmentioning

confidence: 99%

“…Our previous studies in the turkey support the existence of a photoreceptive neuronal group within the premammillary nucleus (PMM) in the caudal MBH [10]. The neuronal group in the PMM is photoreceptive since they express c-fos mRNA in response to a light pulse provided during the photosensitive phase together with the stimulation of gonadotrophin-releasing hormone-I (GnRH-I) neurons in the nucleus commissurae pallii (nCPA) [13].…”

Section: Introductionmentioning

confidence: 99%

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GABAergic Neurotransmission in the Premammillary Nucleus of the Turkey Hypothalamus Regulates Reproductive Seasonality and the Onset of Photorefractoriness

et al. 2015

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Background/Aims: Photoperiod is a major environmental cue in temperate-zone birds which synchronizes breeding with the time of year that offers the optimal environment for offspring survival. Despite continued long photoperiods, these birds eventually become refractory to the stimulating photoperiod and their reproductive systems regress. In this study, we characterized the role of γ-aminobutyric acid (GABA)ergic neurotransmission in modulating the response of the premammillary nucleus (PMM) to a gonad stimulatory photoperiod and the onset of photorefractoriness. Methods and Results: Bilateral ablation of the PMM blocked the light-induced neuroendocrine response from occurring in photosensitive turkeys. Microarray analyses revealed an increase in GABAergic activity in the PMM of photorefractory birds as opposed to photosensitive ones, and this enhanced GABAergic activity appeared to inhibit the photoperiodic signal. Additionally, GABA_A and GABA_B receptors were expressed by dopamine-melatonin neurons in the PMM, and the administration of the GABA receptor agonist baclofen blocked the photoperiodic reproductive neuroendocrine responses. Conclusions: Consistent with the present findings, we propose that the long-sought-after mechanism underlying photorefractoriness is linked to the inhibitory actions of GABA. We suggest that (1) GABAergic interference with photoperiodic entrainment in the PMM initiates the photorefractory state and terminates the annual breeding season in temperate-zone birds, and (2) the PMM is a site of photoreception and photorefractoriness that controls the initiation and termination of avian reproductive seasonality.

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“…Currently 4 sites in the avian brain have been proposed to house DBP ( Figure 2B): 1) the lateral septal region including the lateral septal organ (LSO; Silver et al, 1988;Kuenzel, 1993;Kuenzel and Blähser, 1994;Saldanha et al, 1994;Kuenzel et al, 1997;Wada et al, 2000;Saldanha et al, 2001;Li et al, 2004;Chaurasia et al, 2005;Rathinam and Kuenzel, 2005;Li and Kuenzel, 2008), 2) the PVN (Soni and Foster, 1997;Tomonari et al, 2007;Halford et al, 2009;Davies et al, 2012), 3) premammillary nucleus (PMM; Kang et al, 2007Kang et al, , 2009Kang et al, , 2010Thayananuphat et al, 2007;El Halawani et al, 2009;Kosonsiriluk et al, 2013), and 4) the paraventricular organ (PVO; Vigh-Teichmann et al, 1980;Vigh and Vigh-Teichmann, 1998;. It could be that all 4 brain areas contain DBP and are functionally coordinated to ensure continual function of the essential detection of photoperiodic information.…”

Section: (1) Sensory Photopigment System Involves Deep-brain Photorecmentioning

confidence: 99%

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

Kuenzel¹,

Kang²,

Zhou³

2015

Poultry Science

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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...

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Photoreceptive oscillators within neurons of the premammillary nucleus (PMM) and seasonal reproduction in temperate zone birds

Cited by 28 publications

References 49 publications

The avian ovary and follicle development: some comparative and practical insights

The avian ovary and follicle development: some comparative and practical insights

GABAergic Neurotransmission in the Premammillary Nucleus of the Turkey Hypothalamus Regulates Reproductive Seasonality and the Onset of Photorefractoriness

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

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