Characterization of the Projections to the Hypothalamic Paraventricular and Periventricular Nuclei in the Female Sheep Brain, Using Retrograde Tracing and Immunohistochemistry

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Abstract

The paraventricular nucleus (PVN) and the periventricular nucleus (Pe) are important neuroendocrine centers, but the neuronal input to these regions is poorly defined in nonrodent species. We utilized the retrograde transport of injected tracers to determine the neural input to these two nuclei in the ovine brain. Adult Corriedale ewes were studied following FluoroGold injection into either the PVN (n = 5) or the Pe (n = 3). Both the PVN and the Pe were found to receive neuronal input from a number of hypothalamic nuclei. Projections to the PVN from the lateral hypothalamic area were from neurons that produce melanin-concentrating hormone or orexins and a subset of those from the arcuate nucleus were immunopositive for neuropeptide Y and γ-melanocyte stimulating hormone. This pathway was verified by staining of terminals in the PVN. Input to the PVN from the brain stem was seen to originate from the catecholaminergic and serotoninergic neurons. The projections to the PVN and Pe from hypothalamic and brain stem regions in the sheep brain are generally similar to those in the rat, with some minor differences. These studies highlight the differences in the afferent input to these two closely related nuclei in the ovine brain.

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Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B.

Mohammad R Jafarzadehshirazi, Marco Coolen, Alda Pereira da Silva … (2007)

Kisspeptin is a potent stimulator of GnRH secretion that has been implicated in the feedback actions of ovarian steroids. In ewes, the majority of hypothalamic kisspeptin neurons are found in the arcuate nucleus (ARC), with a smaller population located in the preoptic area. Most arcuate kisspeptin neurons express estrogen receptor-alpha, as do a set of arcuate neurons that contain both dynorphin and neurokinin B (NKB), suggesting that all three neuropeptides are colocalized in the same cells. In this study we tested this hypothesis using dual immunocytochemistry and also determined if kisspeptin neurons contain MSH or agouti-related peptide. To assess colocalization of kisspeptin and dynorphin, we used paraformaldehyde-fixed tissue from estrogen-treated ovariectomized ewes in the breeding season (n = 5). Almost all ARC, but no preoptic area, kisspeptin neurons contained dynorphin. Similarly, almost all ARC dynorphin neurons contained kisspeptin. In experiment 2 we examined colocalization of kisspeptin and NKB in picric-acid fixed tissue collected from ovary intact ewes (n = 9). Over three quarters of ARC kisspeptin neurons also expressed NKB, and a similar percentage of NKB neurons contained kisspeptin. In contrast, no kisspeptin neurons stained for MSH or agouti-related peptide. These data demonstrate that, in the ewe, a high percentage of ARC kisspeptin neurons also produce dynorphin and NKB, and we propose that a single subpopulation of ARC neurons contains all three neuropeptides. Because virtually all of these neurons express estrogen and progesterone re-ceptors, they are likely to relay the feedback effects of these steroids to GnRH neurons to regulate reproductive function.

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The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization.

J Vaughan, Paul E. Sawchenko, F Presse … (1992)

In addition to a nonadecapeptide homologous to the teleost melanin-concentrating hormone (MCH), the amino acid sequence predicted from a rat prepro-MCH (ppMCH) cDNA suggested that at least one (neuropeptide EI, or NEI), and possibly a second (NGE), additional neuropeptide may be encoded by this precursor. Cross-reactivity with epitopes of NEI or NGE can account for reported localization of alpha-MSH, rat CRF, and human GRF in rat dorsolateral hypothalamic neurons. We have used antisera raised against rat MCH and NEI in immunohistochemical studies at the light and electron microscopic levels, along with hybridization histochemical localization of ppMCH mRNA, to define the organization of this system. As expected, ppMCH mRNA is prominently expressed in cells in the lateral hypothalamic area and zona incerta. The MCH and NEI peptides were extensively colocalized in neurons in both of these areas. In addition, smaller cell groups in the olfactory tubercle and pontine tegmentum were also positively hybridized for ppMCH mRNA and immunostained for MCH and NEI. Fibers stained for MCH and NEI were similarly, and very broadly, distributed throughout the central nervous system in patterns that generally conformed with known projection fields of the lateral hypothalamic area and zona incerta. A differential distribution was seen in at least one region, the interanterodorsal nucleus of the thalamus, which contained a prominent terminal field stained for MCH but not NEI. At the electron microscopic level, MCH-stained perikarya displayed a prominent staining associated with the Golgi apparatus; this was not encountered in NEI-stained cells. Both peptides were distributed similarly in terminals in the lateral hypothalamic area and median eminence, with staining associated principally with dense-cored vesicles. The results suggest that ppMCH-derived peptides may serve as neurotransmitters or modulators of prominence in a surprisingly expansive projection field of incerto-hypothalamic neurons. The terminal distributions of this system seem most compatible with functional roles in generalized arousal and sensorimotor integration, processes previously implicated as being subject to modulation by the lateral hypothalamic area.

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Efferent connections of the parabrachial nucleus in the rat.

C.B. Saper, A.D. Loewy (1980)

The efferent connections of the parabrachial nucleus have been analyzed in the rat using the anterograde autoradiographic method. Fibers originating from the lateral parabrachial nucleus (PBl) ascend in the periventricular system, the dorsal tegmental bundle and the central tegmental tract. The PBl projects to the dorsal raphe nucleus, the superior central raphe nucleus, and the Edinger-Westphal nucleus. It also innervates the intralaminar (centromedian, centrolateral, paracentral, parafascicular), the midline (paraventricular, reuniens), and the ventromedial basal (VMb) thalamic nuclei as well as much of the hypothalamus, including the dorsomedial, the ventromedial, the arcuate and the paraventricular nuclei, the lateral hypothalamic and the lateral preoptic areas. The PBl sends fibers via the ansa peduncularis into the amygdala, innervating the anterior, the central, the medial, the basomedial, and the posterior basolateral nuclei. In addition, it projects to the lateral part of the bed nucleus of the stria terminalis. Descending PBl fibers travel mainly through the ventrolateral medulla, passing through the region of the A1 and A5 catecholamine cell groups, the ventrolateral reticular formation and the region that contains parasympathetic preganglionic neurons. A small component travels in Probst's bundle to the ventral part of the nucleus of the solitary tract. Only a few PBl axons continue caudally into the lateral funiculus of the spinal cord, but these could not be followed beyond the first few cervical segments. The projections of the medial parabrachial nucleus (PBm) are similar to those of PBl, but two major differences have been noted. One difference is that the PBm provides a direct input to 4 regions of cerebral cortex: (1) the granular insular cortex; (2) the deep layers of the frontal cortex; (3) the septo-olfactory area; and (4) the infralimbic cortex. The other difference is that unlike the PBl, the PBm appears to provide almost no input to the medial hypothalamic nuclei (dorsomedial, ventromedial, arcuate nuclei) nor to the medial amygdaloid nucleus. The PBm projects heavily to the nucleus ambiguus and there was no evidence for an input to the nucleus of the solitary tract. The projections of the Kölliker-Fuse nucleus (KF) are distinct from those of either PBm or PBl. The KF projects via the central tegmental tract to the lateral hypothalamic area, the lateral preoptic area, and the central nucleus of the amygdala. The contralateral projection to the zona incerta, the lateral hypothalamic area, and the lateral preoptic areas is more prominent than the ipsilateral projections. Descending KF fibers travel mainly through the ventrolateral medullary reticular formation passing through regions which give rise to parasympathetic preganglionic fibers of the VIIth, IXth and Xth cranial nerves and the A1 and A5 catecholamine cell groups. In one experiment, fibers could be followed to the intermediolateral cell column of the upper thoracic spinal cord.

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Author and article information

Journal

Journal ID (publisher-id): NEN

Journal ID (nlm-ta): Neuroendocrinology

Journal ID (doi): 10.1159/issn.0028-3835

Title: Neuroendocrinology

Publisher: S. Karger AG

ISSN (Print): 0028-3835

ISSN (Electronic): 1423-0194

Publication date Subscription-year: 2009

Publication date (Print): July 2009

Publication date (Electronic): 27 May 2009

Volume: 90

Issue: 1

Pages: 31-53

Affiliations

^aDepartment of Physiology, Monash University, Clayton, Vic.,Australia; ^bDepartment of Anatomical Science, Shiraz University of Medical Sciences, Shiraz, Iran

Article

Publisher ID: 221304 Other ID: Neuroendocrinology 2009;90:31–53

DOI: 10.1159/000221304

PubMed ID: 19478473

SO-VID: d03a3154-b148-4c58-9d98-4c0bcab05c45

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Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

History

Date received : 23 September 2008

Date accepted : 12 November 2008

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Figures: 7, Tables: 2, References: 126, Pages: 23

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Characterization of the Projections to the Hypothalamic Paraventricular and Periventricular Nuclei in the Female Sheep Brain, Using Retrograde Tracing and Immunohistochemistry

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Karger: Endocrinology

Most cited references 100

Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B.

The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization.

Efferent connections of the parabrachial nucleus in the rat.

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