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A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys

ABSTRACT: Motivation boosts motor performance. Activity of the ventral midbrain (VM), consisting of the ventral tegmental area (VTA), the substantia nigra pars compacta (SNc) and the retrorubral field (RRF), plays an important role in processing motivation. However, little is known about the neural...

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Autores principales: Suzuki, Michiaki, Inoue, Ken‐ichi, Nakagawa, Hiroshi, Ishida, Hiroaki, Kobayashi, Kenta, Isa, Tadashi, Takada, Masahiko, Nishimura, Yukio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306604/
https://www.ncbi.nlm.nih.gov/pubmed/35122444
http://dx.doi.org/10.1113/JP282429
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author Suzuki, Michiaki
Inoue, Ken‐ichi
Nakagawa, Hiroshi
Ishida, Hiroaki
Kobayashi, Kenta
Isa, Tadashi
Takada, Masahiko
Nishimura, Yukio
author_facet Suzuki, Michiaki
Inoue, Ken‐ichi
Nakagawa, Hiroshi
Ishida, Hiroaki
Kobayashi, Kenta
Isa, Tadashi
Takada, Masahiko
Nishimura, Yukio
author_sort Suzuki, Michiaki
collection PubMed
description ABSTRACT: Motivation boosts motor performance. Activity of the ventral midbrain (VM), consisting of the ventral tegmental area (VTA), the substantia nigra pars compacta (SNc) and the retrorubral field (RRF), plays an important role in processing motivation. However, little is known about the neural substrate bridging the VM and the spinal motor output. We hypothesized that the VM might exert a modulatory influence over the descending motor pathways. By retrograde transneuronal labelling with rabies virus, we demonstrated the existence of multisynaptic projections from the VM to the cervical enlargement in monkeys. The distribution pattern of spinal projection neurons in the VM exhibited a caudorostral gradient, in that the RRF and the caudal part of the SNc contained more retrogradely labelled neurons than the VTA and the rostral part of the SNc. Electrical stimulation of the VM induced muscle responses in the contralateral forelimb with a delay of a few milliseconds following the responses of the ipsilateral primary motor cortex (M1). The magnitude and number of evoked muscle responses were associated with the stimulus intensity and number of pulses. The muscle responses were diminished during M1 inactivation. Thus, the present study has identified a multisynaptic VM–spinal pathway that is mediated, at least in part, by the M1 and might play a pivotal role in modulatory control of the spinal motor output. KEY POINTS: Motivation to obtain reward is thought to boost motor performance, and activity in the ventral midbrain is important to the motivational process. Little is known about a neural substrate bridging the ventral midbrain and the spinal motor output. Retrograde trans‐synaptic experiments revealed that the ventral midbrain projects multisynaptically to the spinal cord in macaque monkeys. Ventral midbrain activation by electrical stimulation generated cortical activity in the motor cortex and forelimb muscle activity. A multisynaptic ventral midbrain–spinal pathway most probably plays a pivotal role in modulatory control of the spinal motor output.
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spelling pubmed-93066042022-07-28 A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys Suzuki, Michiaki Inoue, Ken‐ichi Nakagawa, Hiroshi Ishida, Hiroaki Kobayashi, Kenta Isa, Tadashi Takada, Masahiko Nishimura, Yukio J Physiol Neuroscience ABSTRACT: Motivation boosts motor performance. Activity of the ventral midbrain (VM), consisting of the ventral tegmental area (VTA), the substantia nigra pars compacta (SNc) and the retrorubral field (RRF), plays an important role in processing motivation. However, little is known about the neural substrate bridging the VM and the spinal motor output. We hypothesized that the VM might exert a modulatory influence over the descending motor pathways. By retrograde transneuronal labelling with rabies virus, we demonstrated the existence of multisynaptic projections from the VM to the cervical enlargement in monkeys. The distribution pattern of spinal projection neurons in the VM exhibited a caudorostral gradient, in that the RRF and the caudal part of the SNc contained more retrogradely labelled neurons than the VTA and the rostral part of the SNc. Electrical stimulation of the VM induced muscle responses in the contralateral forelimb with a delay of a few milliseconds following the responses of the ipsilateral primary motor cortex (M1). The magnitude and number of evoked muscle responses were associated with the stimulus intensity and number of pulses. The muscle responses were diminished during M1 inactivation. Thus, the present study has identified a multisynaptic VM–spinal pathway that is mediated, at least in part, by the M1 and might play a pivotal role in modulatory control of the spinal motor output. KEY POINTS: Motivation to obtain reward is thought to boost motor performance, and activity in the ventral midbrain is important to the motivational process. Little is known about a neural substrate bridging the ventral midbrain and the spinal motor output. Retrograde trans‐synaptic experiments revealed that the ventral midbrain projects multisynaptically to the spinal cord in macaque monkeys. Ventral midbrain activation by electrical stimulation generated cortical activity in the motor cortex and forelimb muscle activity. A multisynaptic ventral midbrain–spinal pathway most probably plays a pivotal role in modulatory control of the spinal motor output. John Wiley and Sons Inc. 2022-02-17 2022-04-01 /pmc/articles/PMC9306604/ /pubmed/35122444 http://dx.doi.org/10.1113/JP282429 Text en © 2022 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Neuroscience
Suzuki, Michiaki
Inoue, Ken‐ichi
Nakagawa, Hiroshi
Ishida, Hiroaki
Kobayashi, Kenta
Isa, Tadashi
Takada, Masahiko
Nishimura, Yukio
A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys
title A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys
title_full A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys
title_fullStr A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys
title_full_unstemmed A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys
title_short A multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys
title_sort multisynaptic pathway from the ventral midbrain toward spinal motoneurons in monkeys
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306604/
https://www.ncbi.nlm.nih.gov/pubmed/35122444
http://dx.doi.org/10.1113/JP282429
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