Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds

Kang, Seong Wook; Leclerc, B.; Kosonsiriluk, Sunantha; Mauro, Laura J.; Iwasawa, Atsushi; Halawani, Mohamed E. El

doi:10.1016/j.neuroscience.2010.06.082

Cited by 73 publications

(74 citation statements)

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“…Dopamine (DA) and the hormonal synchronizer of the circadian oscillators, melatonin (Mel), are colocalized within the PMM and exhibit a daily endogenous dual oscillation in DAergic/MELergic activities [14]. The established pathway from the PMM to the pars tuberalis (PT) [15] suggests that the output of the photoperiodic signal is transmitted to the neuroendocrine system cascade that facilitates the release of GnRH-I. Indeed, the photic input for circadian photoentrainment is detected by melanopsin and measured by clock genes localized within DA-Mel neurons in the PMM [15,16].…”

Section: Introductionmentioning

confidence: 99%

“…The established pathway from the PMM to the pars tuberalis (PT) [15] suggests that the output of the photoperiodic signal is transmitted to the neuroendocrine system cascade that facilitates the release of GnRH-I. Indeed, the photic input for circadian photoentrainment is detected by melanopsin and measured by clock genes localized within DA-Mel neurons in the PMM [15,16]. The encoded photoperiodic information is transmitted via the DAergic system to the PT of the endocrine system as DAergic fibers from PMM DA-Mel neurons project to the PT [15].…”

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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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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“…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%

“…To date, however, which sites are critical and how they communicate among themselves remain unknown. Each of the 4 neural loci proposed to house DBP is in different brain structures, and 3 distinct photopigments have been discovered and thought involved in the reception of photoperiodic information: melanopsin/Opn4 (Chaurasia et al, 2005;Kang et al, 2010), neuropsin/Opn5 Ohuchi et al, 2012), and vertebrate ancient opsin (VAOpn; Foster et al, 1985Foster et al, , 1994Halford et al, 2009;Davies et al, 2012).…”

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

confidence: 99%

“…The MidHypo contains VAOpn (Halford et al, 2009) neurons in the PVN and medial bed nucleus of the stria terminalis. The Post-Hypo region ( Figure 2B) contains Opn4 neurons in the PMM (Kang et al, 2010) and Opn5 neurons in the PVO . In addition, the anterior pituitary was dissected and frozen while the testes were sampled and weighed.…”

Section: Multiple Brain Sites Containing Functional Dbpmentioning

confidence: 99%

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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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Comparative analysis of monoaminergic cerebrospinal fluid‐contacting cells in Osteichthyes (bony vertebrates)

Xavier

Fontaine

Bloch

et al. 2017

J of Comparative Neurology

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Cerebrospinal fluid-contacting (CSF-c) cells containing monoamines such as dopamine (DA) and serotonin (5-HT) occur in the periventricular zones of the hypothalamic region of most vertebrates except for placental mammals. Here we compare the organization of the CSF-c cells in chicken, Xenopus, and zebrafish, by analyzing the expression of synthetic enzymes of DA and 5-HT, respectively, tyrosine hydroxylase (TH) and tryptophan hydroxylase (TPH), and draw an evolutionary scenario for this cell population. Due to the lack of TH immunoreactivity in this region, the hypothalamic CSF-c cells have been thought to take up DA from the ventricle instead of synthesizing it. We demonstrate that a second TH gene (TH2) is expressed in the CSF-c cells of all the three species, suggesting that these cells do indeed synthetize DA. Furthermore, we found that many CSF-c cells coexpress TH2 and TPH1 and contain both DA and 5-HT, a dual neurotransmitter phenotype hitherto undescribed in the brain of any vertebrate. The similarities of CSF-c cells in chicken, Xenopus, and zebrafish suggest that these characteristics are inherited from the common ancestor of the Osteichthyes. A significant difference between tetrapods and teleosts is that teleosts possess an additional CSF-c cell population around the posterior recess (PR) that has emerged in specific groups of Actinopterygii. Our comparative analysis reveals that the hypothalamus in mammals and teleosts has evolved in a divergent manner: placental mammals have lost the monoaminergic CSF-c cells, while teleosts have increased their relative number. K E Y W O R D S

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Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds

Cited by 73 publications

References 50 publications

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

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

Comparative analysis of monoaminergic cerebrospinal fluid‐contacting cells in Osteichthyes (bony vertebrates)

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