A novel developmental critical period of orexinergic signaling in the primary visual thalamus

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Summary

The orexinergic system of the lateral hypothalamus plays crucial roles in arousal, feeding behavior, and reward modulation. Most research has focused on adult rodents, overlooking orexins’ potential role in the nervous system development. This study, using electrophysiological and molecular tools, highlights importance of orexinergic signaling in the postnatal development of the rodent dorsolateral geniculate nucleus (DLG), a primary visual thalamic center. Orexin activation of DLG thalamocortical neurons occurs in a brief seven-day window around eye-opening, concurrent to transient OX ₂ receptor expression. Blocking OX ₂ receptors during this period reduces sensitivity of DLG neurons to green and blue light and lowers spontaneous firing rates in adulthood. This research reveals critical and temporally confined role of orexin signaling in postnatal brain development, emphasizing its contribution to experience-dependent refinement in the DLG and its long-term impact on visual function.

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Highlights

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Sensitivity to OXA was studied in the rodent dorsolateral geniculate (DLG) nucleus
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DLG neurons respond to OXA within a week-long period around eye-opening
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This coincides with developmental window in OX ₂ receptor expression
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Blocking OX ₂ receptors in pups impairs visual processing in adulthood

Abstract

Optical signal processing; Neuroscience; Behavioral neuroscience

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Differential expression of orexin receptors 1 and 2 in the rat brain.

J. Marcus, C Aschkenasi, C. Lee … (2001)

Orexins (hypocretins) are neuropeptides synthesized in the central nervous system exclusively by neurons of the lateral hypothalamus. Orexin-containing neurons have widespread projections and have been implicated in complex physiological functions including feeding behavior, sleep states, neuroendocrine function, and autonomic control. Two orexin receptors (OX(1)R and OX(2)R) have been identified, with distinct expression patterns throughout the brain, but a systematic examination of orexin receptor expression in the brain has not appeared. We used in situ hybridization histochemistry to examine the patterns of expression of mRNA for both orexin receptors throughout the brain. OX(1)R mRNA was observed in many brain regions including the prefrontal and infralimbic cortex, hippocampus, paraventricular thalamic nucleus, ventromedial hypothalamic nucleus, dorsal raphe nucleus, and locus coeruleus. OX(2)R mRNA was prominent in a complementary distribution including the cerebral cortex, septal nuclei, hippocampus, medial thalamic groups, raphe nuclei, and many hypothalamic nuclei including the tuberomammillary nucleus, dorsomedial nucleus, paraventricular nucleus, and ventral premammillary nucleus. The differential distribution of orexin receptors is consistent with the proposed multifaceted roles of orexin in regulating homeostasis and may explain the unique role of the OX(2)R receptor in regulating sleep state stability. Copyright 2001 Wiley-Liss, Inc.

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Neurons containing hypocretin (orexin) project to multiple neuronal systems.

Christelle Peyron, Devin K. Tighe, Anthony van den Pol … (1998)

The novel neuropeptides called hypocretins (orexins) have recently been identified as being localized exclusively in cell bodies in a subregion of the tuberal part of the hypothalamus. The structure of the hypocretins, their accumulation in vesicles of axon terminals, and their excitatory effect on cultured hypothalamic neurons suggest that the hypocretins function in intercellular communication. To characterize these peptides further and to help understand what physiological functions they may serve, we undertook an immunohistochemical study to examine the distribution of preprohypocretin-immunoreactive neurons and fibers in the rat brain. Preprohypocretin-positive neurons were found in the perifornical nucleus and in the dorsal and lateral hypothalamic areas. These cells were distinct from those that express melanin-concentrating hormone. Although they represent a restricted group of cells, their projections were widely distributed in the brain. We observed labeled fibers throughout the hypothalamus. The densest extrahypothalamic projection was found in the locus coeruleus. Fibers were also seen in the septal nuclei, the bed nucleus of the stria terminalis, the paraventricular and reuniens nuclei of the thalamus, the zona incerta, the subthalamic nucleus, the central gray, the substantia nigra, the raphe nuclei, the parabrachial area, the medullary reticular formation, and the nucleus of the solitary tract. Less prominent projections were found in cortical regions, central and anterior amygdaloid nuclei, and the olfactory bulb. These results suggest that hypocretins are likely to have a role in physiological functions in addition to food intake such as regulation of blood pressure, the neuroendocrine system, body temperature, and the sleep-waking cycle.

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Author and article information

Contributors

Mino D.C. Belle

Marian H. Lewandowski

Lukasz Chrobok

Journal

Journal ID (nlm-ta): iScience

Journal ID (iso-abbrev): iScience

Title: iScience

Publisher: Elsevier

ISSN (Electronic): 2589-0042

Publication date PMC-release: 24 June 2024

Publication date Collection: 19 July 2024

Publication date (Electronic): 24 June 2024

Volume: 27

Issue: 7

Electronic Location Identifier: 110352

Affiliations

[1 ]Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Krakow, Poland

[2 ]Institute for Systems Physiology, University of Cologne, Cologne, Germany

[3 ]Max-Delbrueck-Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany

[4 ]Department of Glycoconjugate Biochemistry, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Krakow, Poland

[5 ]Department of Inorganic Chemistry, Analytical Chemistry and Electrochemistry, Faculty of Chemistry, Silesian University of Technology, Gliwice, Poland

[6 ]The Biotechnology Centre, Silesian University of Technology, Gliwice, Poland

[7 ]Division of Neuroscience, School of Biological Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, Manchester, UK

[8 ]University of Exeter Medical School, Hatherly Labs, Streatham Campus, Prince of Wales Road, Exeter, Devon, UK

[9 ]School of Physiology, Pharmacology, and Neuroscience, Faculty of Health and Life Sciences, University of Bristol, Bristol, UK

[10 ]Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK

Author notes

[∗ ]Corresponding author mino.belle@ 123456manchester.ac.uk

[∗∗ ]Corresponding author marian.lewandowski@ 123456uj.edu.pl

[∗∗∗ ]Corresponding author lukasz.chrobok@ 123456bristol.ac.uk

[11]

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Article

Publisher Item ID: S2589-0042(24)01577-3 Publisher ID: 110352

DOI: 10.1016/j.isci.2024.110352

PMC ID: 11269934

PubMed ID: 39055917

SO-VID: 4527dcdd-00ba-4e37-ba66-3ac02c0cca79

License:

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

History

Date received : 12 January 2024

Date revision received : 15 April 2024

Date accepted : 20 June 2024

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A novel developmental critical period of orexinergic signaling in the primary visual thalamus

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Most cited references 69

ggfortify: Unified Interface to Visualize Statistical Results of Popular R Packages

Differential expression of orexin receptors 1 and 2 in the rat brain.

Neurons containing hypocretin (orexin) project to multiple neuronal systems.

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