Postnatal development of the suprachiasmatic nucleus in the rat. Morpho-functional characteristics and time course of tyrosine hydroxylase immunopositive fibers

Beltramo, Massimiliano; Calas, A.; Chernigovskaya, E. V.; Borisova, N. A.; Polenova, O.; Tillet, Yves; Thibault, Jean; Ugrumov, M. V.

doi:10.1016/0306-4522(94)90553-3

Cited by 30 publications

(21 citation statements)

References 22 publications

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“…This transient catecholamine input to the SCN has also been observed in the rat (Ugrumov et al, 1989a;Beltramo et al, 1994) and very recently in the Syrian hamster (Strother et al, 1998a). Ugrumov et al and Beltramo et al described TH-ir fibres first appearing on PD2 in the SCN with a similar pattern to that observed in the current study, that is, with the greatest density in the ventromedial region of the middle and caudal SCN.…”

Section: Discussionsupporting

confidence: 83%

“…It is possible that either these or extrahypothalamic neurones entering the hypothalamus through the medial forebrain bundle (Reisert et al, 1990;Borisova et al, 1991) innervate the SCN with their axons and terminals. The distribution pattern of TH-ir fibres in the SCN is similar to that of serotonin (5-HT)-ir fibres, as observed in the postnatal and adult rat and in the adult Syrian hamster (Moore et al, 1978;van den Pol and Tsujimoto, 1985;Beltramo et al, 1994;Ugrumov et al, 1994b;Takatsuji et al, 1995;Hastings et al, 1996). Beltramo et al used a selective neurochemical lesion approach to investigate whether TH and 5-HT are colocalised in fibres in the SCN in the PD10 rat.…”

Section: Discussionmentioning

confidence: 84%

“…Thus, it is possible that, in the case of the developing SCN, the period prior to TH-ir fibre innervation represents a ''supersensitive'' state (Robertson et al, 1989;Marshall, 1992, 1994), and catecholamine fibre innervation during the perinatal period both may provide a mechanism for entrainment and may desensitise the dopamine transduction pathways in the SCN. This hypothesis might also explain the paradox in the neonatal rat SCN between the reported ''late'' arrival of the TH-ir fibre plexus (Beltramo et al, 1994) and the ability of SKF 38393 to induce c-fos in the SCN during the late foetal and early postnatal period (Weaver et al, 1992;.…”

Section: Discussionmentioning

confidence: 98%

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Anatomical and functional characterisation of a dopaminergic system in the suprachiasmatic nucleus of the neonatal siberian hamster

1999

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In altricial rodents, maternal influences entrain the developing circadian system in the perinatal period before the capacity to respond directly to photic cues develops. The aim of these studies was to investigate the potential role of dopamine in this process in the Siberian hamster. An initial study investigated the ontogeny of retinal innervation of the suprachiasmatic nuclei (SCN) by using cholera toxin B subunit as a tracer. This revealed that retinal fibres first innervate the SCN on postnatal day 3 (PD3), and ingrowth of fibres is extensive by PD6. In situ hybridisation studies revealed the presence of D1‐dopamine receptor (D1‐R) mRNA in the SCN on PD2, and levels of expression were similar in PD6 pups and adult hamsters. Immunocytochemical staining for tyrosine hydroxylase revealed abundant catecholaminergic fibres within the ventromedial zone of the SCN from the day of birth through PD20; however, in contrast, few fibres were present in adult SCN. Dopamine‐β‐hydroxylase‐immunoreactive fibres were absent from the neonatal and adult SCN, suggesting that the fibres in the SCN are dopaminergic. The function of this dopaminergic system was investigated by determining the effects of D1‐R agonists on the expression of the immediate‐early gene c‐fos in the SCN. This was assessed in pups ages PD1– PD5 by in situ hybridisation and immunocytochemical localisation of its protein product. No induction was seen in the SCN, in marked contrast to studies in the developing rat. A final series of studies investigated dopaminergic function by determining whether a D1‐agonist could induce phosphorylation of Ca2+/cyclic AMP response element‐binding protein (CREB) on Ser133. Hypothalamic slices containing SCN taken from PD1 and PD2 hamsters were treated with D1‐R agonists, and levels of phosphorylated CREB were assayed by Western blots. Phosphorylation of CREB was stimulated by D1‐R agonists in both Syrian and Siberian hamster hypothalamus, but the response was far greater in Syrian hamster tissue (+138% ± 28%) than in Siberian hamster tissue (+43% ± 11%). Although the anatomical studies demonstrate the existence of a dopaminergic system in the SCN of the early postnatal Siberian hamster, the unresponsiveness of c‐fos expression and the relative lack of phosphorylation of CREB after D1‐R activation suggests a diminished role for dopamine in the regulation of circadian events during the postnatal period in this species. J. Comp. Neurol. 408:73–96, 1999. © 1999 Wiley‐Liss, Inc.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 84%

Section: Discussionmentioning

confidence: 98%

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Anatomical and functional characterisation of a dopaminergic system in the suprachiasmatic nucleus of the neonatal siberian hamster

1999

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“…The materials of the experimental and control animals were processed under standardized conditions (fixation, sectioning and immunostaining) that made it possible to compare the concentrations of the immunoreactive materials in individual neurons and mRNAs in the whole SON by measuring OD (Smolen 1990). The validity of these techniques has been repeatedly demonstrated in earlier studies (Beltramo et al 1994(Beltramo et al , 1997Abramova et al 2002;Mirochnik et al 2005).…”

Section: Technical Remarksmentioning

confidence: 79%

Vasopressinergic neurons of the supraoptic nucleus in perinatal rats: reaction to osmotic stimulation and its regulation

2010

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Osmotic stimulation (OS) of vasopressin (VP) neurons of the supraoptic nucleus (SON) promotes VP secretion and tyrosine hydroxylase (TH) expression in adult mammals. VP secretion is under a noradrenaline control, whereas the regulation of TH expression remains uncertain. This study was aimed to determine at what period of ontogenesis: (1) VP neurons begin to react to OS by modifying simultaneously VP and TH gene expression and synthesis, (2) the noradrenergic control of VP neurons is established. Rats on the 21st embryonic day (E), third postnatal day (P), P13 were salt loaded or salt loaded and treated with an antagonist (prazosin) or agonist (phenylephrine) of α1-adrenoreceptors. According to our immunocytochemical and in situ hybridization data, OS resulted in an increased amount of VP mRNA in each age group and of VP on E21 and P3. TH gene and synthesis was initially expressed under OS on P3. The number of TH-expressing neurons diminished by threefold in salt loaded rats from P3 to P13. OS combined with prazosin administration resulted in an increased level of VP mRNA on P3 and P13, but not on E21 suggesting the onset of the noradrenaline inhibitory control after birth. OS together with prazosin treatment stimulated TH expression on P3 and P13, whereas phenylephrine provided an opposite effect. Thus, VP neurons begin to react to OS by an increased VP synthesis at the end of fetal life and by the onset of TH expression shortly after birth; the expression of both substances appears to be under the inhibitory control of noradrenaline.

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“…The time at which human substantia nigra dopaminergic neurons form and, consequently, the optimal time for transplanting them, is determined largely by the onset of TH expression [25]. However, this parameter is not absolutely specific, because TH can be expressed transiently in embryogenesis [7] as well as in neurons lacking aromatic L-amino acid decarboxylase [5,12,14]. These studies were therefore supplemented by identification of the time at which specific reuptake and secretion of dopamine in response to membrane depolarization develop, using a biochemical isotope-based method [23].…”

Section: Differentiation and Transplantation Of Dopaminergic Neurons mentioning

confidence: 99%

The differentiation of dopaminergic neurons in situ, in vivo, and in transplants

Ugryumov

2000

Neurosci Behav Physiol

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This article summarizes results obtained from studies on the differentiation of dopaminergic neurons in animal hypothalamus and human substantia nigra in situ, in vitro, and in transplants, as well as the role of the microenvironment in regulating this process. Four stages were identified in the differentiation of dopaminergic neurons from rat hypothalamus: a) formation of neurons from neuroepithelial precursor cells, b) expression of specific synthetic products (enzymes and dopamine itself) and mechanisms for transmembrane dopamine transport (reuptake and secretion in response to membrane depolarization), c) formation of permanent and transient efferent connections, and d) formation of afferent innervation and synaptogenesis. Along with dopaminergic neurons, rat fetuses contained neurons expressing only one of the dopamine-synthesizing enzymes and probably taking part in in situ dopamine synthesis. Differentiation of dopaminergic neurons was sexually dimorphic in terms of the dynamics of neuron formation and expression of enzymes involved in dopamine synthesis. A neurotransplantation model showed that humoral factors of placental and maternal origin had no significant effect on the differentiation of the dopaminergic neurons of the hypothalamus. As regards the dopaminergic neurons of the substantia nigra, expression of their specific phenotype in human fetuses started with the synthesis of tyrosine hydroxylase and co-maturation of the specific dopamine reuptake mechanism during the sixth week of development. During the next four weeks, specific uptake increased, and this appears to be a measure of the number of neurons and the growth of their processes. These data provide the basis for regarding the period from week 6 to week 10 as optimal for transplantation of dopaminergic neurons into the striatum of patients with Parkinson's disease. Suspensions of fetal substantia nigra cells enriched with dopaminergic neurons were introduced stereotaxically into a patient's striatum through a cannula. Positron emission tomography studies showed that the transplanted neurons survived within the host brain, underwent differentiation, and started to synthesize dopamine. The results of clinical assessment performed in parallel with these studies suggested that the transplanted dopaminergic neurons were involved in regulating striatal target neurons.

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Postnatal development of the suprachiasmatic nucleus in the rat. Morpho-functional characteristics and time course of tyrosine hydroxylase immunopositive fibers

Cited by 30 publications

References 22 publications

Anatomical and functional characterisation of a dopaminergic system in the suprachiasmatic nucleus of the neonatal siberian hamster

Anatomical and functional characterisation of a dopaminergic system in the suprachiasmatic nucleus of the neonatal siberian hamster

Vasopressinergic neurons of the supraoptic nucleus in perinatal rats: reaction to osmotic stimulation and its regulation

The differentiation of dopaminergic neurons in situ, in vivo, and in transplants

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