Distribution of raphespinal fibers in the mouse spinal cord

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Abstract

Background

Serotonergic raphespinal neurons and their fibers have been mapped in large mammals, but the non-serotonergic ones have not been studied, especially in the mouse. The present study aimed to investigate the termination pattern of fibers arising from the hindbrain raphe and reticular nuclei which also have serotonergic neurons by injecting the anterograde tracer BDA into them.

Results

We found that raphespinal fibers terminate in both the dorsal and ventral horns in addition to lamina 10. There is a shift of the fibers in the ventral horn towards the dorsal and lateral part of the gray matter. Considerable variation in the termination pattern also exists between raphe nuclei with raphe magnus having more fibers terminating in the dorsal horn. Fibers from the adjacent gigantocellular reticular nucleus show similar termination pattern as those from the raphe nuclei with slight difference. Immunofluorescence staining showed that raphespinal fibers were heterogeneous and serotoninergic fibers were present in all laminae but mainly in laminae 1, 2, medial lamina 8, laminae 9 and 10. Surprisingly, immunofluorescence staining on clarified spinal cord tissue revealed that serotoninergic fibers formed bundles regularly in a short distance along the rostrocaudal axis in the medial part of the ventral horn and they extended towards the lateral motor neuron column area.

Conclusion

Serotonergic and non-serotonergic fibers arising from the hindbrain raphe and reticular nuclei had similar termination pattern in the mouse spinal cord with subtle difference. The present study provides anatomical foundation for the multiple roles raphe and adjacent reticular nuclei play.

Electronic supplementary material

The online version of this article (doi:10.1186/s12990-015-0046-x) contains supplementary material, which is available to authorized users.

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Most cited references 43

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The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat.

B. E. Jones, T. Z. Yang (1985)

Following injections of [3H]leucine into the formatio reticularis gigantocellularis (Rgc), reticularis pontis caudalis (Rpc), reticularis pontis oralis (Rpo), reticularis mesencephali (Rmes), or the locus coeruleus (LC) of the rat, autoradiographic study revealed prominent reticuloreticular projections from all areas and secondary projections onto cranial nerve motor nuclei from most areas within the brain stem. Common long descending projections extended the full length of the spinal cord terminating in the ventromedial ventral horn and intermediate zone and more sparsely in the base of the dorsal horn and (particularly from Rgc) the region of the motoneurons. Common long ascending projections extended into the forebrain via Forel's tegmental fascicles. A dorsal branch of fibers innervated the intralaminar and midline nuclei of the thalamus. The major fiber system continued forward through Forel's fields and ascended into the pallidum from Rpo, Rmes, and LC and into the neostriatum from Rmes and LC. Fascicles from all areas also ascended in the medial forebrain bundle through the lateral hypothalamus to the lateral preoptic area, substantia innominata, and nuclei of the diagonal band. From Rpo, Rmes, and LC, fibers continued forward to reach the cerebral cortex, where the innervation was sparse and discrete from Rpo and Rmes but moderate and ubiquitous from LC. Retrograde transport of true blue and/or nuclear yellow revealed inverse gradients along the brain stem longitudinal axis of interdigitated cells respectively projecting caudally into the spinal cord (with the greatest number of cells in Rgc, Rpc, and Rpo) and rostrally into the diencephalon (with the greatest number of cells in Rmes and LC), with very few cells projecting both to the spinal cord and the diencephalon. From the basal forebrain, a large number of reticular and LC cells were retrogradely labelled, whereas from the frontal cortex, a much smaller number of reticular cells was labelled. These results document the widespread efferent projections from the reticular formation and overlapping, yet more extensive, projections from the LC.

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Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan.

J. Hounsgaard, H Hultborn, B Jespersen … (1988)

1. In the preceding paper (Crone, Hultborn, Kiehn, Mazieres & Wigström, 1988) it was shown that a short-lasting synaptic excitation ('on' stimulus) of extensor motoneurones (primarily triceps surae) in the decerebrate cat often resulted in a maintained excitability increase, which could be reset by a short-lasting inhibitory stimulus train ('off' stimulus). In the present experiments intracellular recording from triceps surae motoneurones and the electroneurogram (ENG activity) from triceps surae nerve branches were performed in parallel. 2. Sustained firing of individual triceps surae motoneurones was most often recorded in parallel with the maintained ENG activity following a synaptic 'on' stimulus. When the motoneurone was silenced, by a hyperpolarizing current through the microelectrode, there was no sign of on-going synaptic excitation during the maintained ENG activity following an 'on' stimulus. It was therefore suggested that voltage-dependent intrinsic properties of the motoneurones themselves could be responsible for the maintained firing. 3. In confirmation of this hypothesis it was found that short-lasting depolarizing current pulses through the recording microelectrode could trigger a self-sustained firing in the motoneurone provided that the bias current (i.e. the holding potential) was kept within certain limits. Hyperpolarizing current pulses terminated the firing. When the spike-generating mechanism was inactivated (by long-lasting excessive depolarization) similar depolarizing and hyperpolarizing current pulses could initiate and terminate plateau potentials in the motoneurones. By grading the depolarizing current pulses it was found that the plateau potentials were of all-or-none character, typically around 10 mV in amplitude. The two levels of excitability which can be triggered by short-lasting excitation and inhibition of the motoneurones is referred to as 'bistable' behaviour of the motoneurones. 4. After an acute spinal transection, in the unanaesthetized cat, the bistable behaviour of the motoneurones disappeared. However, it reappears following intravenous injection of the serotonin precursor 5-hydroxytryptophan (50-120 mg/kg). 5. Individual triceps surae motor units were recorded by selective EMG electrodes during tonic stretch reflexes in the decerebrate preparations. Based on an analysis of their firing pattern during lengthening and shortening (or vibration) of the muscle it is suggested that plateau potentials in motoneurones are recruited during the tonic stretch reflex. Furthermore, it is argued that a quantitatively important part of the depolarization of motoneurones during the tonic stretch reflex indeed originates from these plateau potentials.(ABSTRACT TRUNCATED AT 400 WORDS)

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Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat.

M Zhuo, G F Gebhart (1997)

The modulatory effects of electrical and chemical (glutamate) stimulation in the rostral ventromedial medulla (RVM) on spinal nociceptive transmission and a spinal nociceptive reflex were studied in rats. Electrical stimulation at a total 86 sites in the RVM in the medial raphe nuclei (n = 54) and adjacent gigantocellular areas (n = 32) produced biphasic (facilitatory and inhibitory, n = 43) or only inhibitory (n = 43) modulation of the tail-flick (TF) reflex. At these 43 biphasic sites in the RVM, facilitation of the TF reflex was produced at low intensities of stimulation (5-25 microA) and inhibition was produced at greater intensities of stimulation (50-200 microA). At 43 sites in the RVM, electrical stimulation only produced intensity-dependent inhibition of the TF reflex. Activation of cell bodies in the RVM by glutamate microinjection reproduced the biphasic modulatory effects of electrical stimulation. At biphasic sites previously characterized by electrical stimulation, glutamate at a low concentration (5 nmol) produced facilitation of the TF reflex; a greater concentration (50 nmol) only inhibited the TF reflex. In electrophysiological experiments, electrical stimulation at 62 sites in the RVM produced biphasic (n = 26), only inhibitory (n = 26), or only facilitatory (n = 10) modulation of responses of lumbar spinal dorsal horn neurons to noxious cutaneous thermal (50 degrees C) or mechanical (75.9 g) stimulation. Facilitatory effects were produced at lesser intensities of stimulation and inhibitory effects were produced at greater intensities of stimulation. The apparent latencies to stimulation-produced facilitation and inhibition, determined with the use of a cumulative sum method and bin-by-bin analysis of spinal neuron responses to noxious thermal stimulation of the skin, were 231 and 90 ms, respectively. The spinal pathways conveying descending facilitatory and inhibitory influences were found to be different. Descending facilitatory influences on the TF reflex were conveyed in ventral/ventrolateral funiculi, whereas inhibitory influences were conveyed in dorsolateral funiculi. The results indicate that descending inhibitory and facilitatory influences can be simultaneously engaged throughout the RVM, including nucleus raphe magnus, and that such influences are conveyed in different spinal funiculi.

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Author and article information

Contributors

Huazheng Liang: h.liang@neura.edu.au

Shaoshi Wang: wangshaoshi@126.com

Richard Francis: richard.francis@unsw.edu.au

Renee Whan: r.whan@unsw.edu.au

Charles Watson: c.watson@curtin.edu.au

George Paxinos: g.paxinos@neura.edu.au

Journal

Journal ID (nlm-ta): Mol Pain

Journal ID (iso-abbrev): Mol Pain

Title: Molecular Pain

Publisher: BioMed Central (London )

ISSN (Electronic): 1744-8069

Publication date (Electronic): 16 July 2015

Publication date PMC-release: 16 July 2015

Publication date Collection: 2015

Volume: 11

Electronic Location Identifier: 42

Affiliations

[ ]Neuroscience Research Australia, 139 Barker Street, Randwick, NSW 2031 Australia

[ ]Department of Neurology, Branch of Shanghai First People’s Hospital, Shanghai, 200081 China

[ ]Biomedical Imaging Facility, The University of New South Wales, Sydney, NSW 2052 Australia

[ ]Health Sciences Dean Research, Faculty of Health Sciences, Curtin University, Shenton Park Campus, Perth, WA 6102 Australia

[ ]School of Medical Sciences, The University of New South Wales, Sydney, NSW 2052 Australia

Article

Publisher ID: 46

DOI: 10.1186/s12990-015-0046-x

PMC ID: 4502924

PubMed ID: 26173454

SO-VID: 9fdaf395-7560-4cba-bd9e-314b6a0e2510

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 18 April 2015

Date accepted : 3 July 2015

Custom metadata

ScienceOpen disciplines: Molecular medicine

Keywords: hindbrain,raphe nuclei,reticular nuclei,serotonin,spinal cord,raphespinal tract,clarity,anterograde tracing

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ScienceOpen disciplines: Molecular medicine

Keywords: hindbrain, raphe nuclei, reticular nuclei, serotonin, spinal cord, raphespinal tract, clarity, anterograde tracing

Distribution of raphespinal fibers in the mouse spinal cord

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Results

Conclusion

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Most cited references 43

The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat.

Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan.

Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat.

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