Parallel descending dopaminergic connectivity of A13 cells to the brainstem locomotor centers

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Abstract

The mesencephalic locomotor region (MLR) is an important integrative area for the initiation and modulation of locomotion. Recently it has been realized that dopamine (DA) projections from the substantia nigra pars compacta project to the MLR. Here we explore DA projections from an area of the medial zona incerta (ZI) known for its role in motor control onto the MLR. We provide evidence that dopaminergic (DAergic) A13 neurons have connectivity to the cuneiform nucleus (CnF) and pedunculopontine tegmental nucleus (PPTg) of the MLR. No ascending connectivity to the dorsolateral striatum was observed. On the other hand, DAergic A13 projections to the medullary reticular formation (MRF) and the lumbar spinal cord were sparse. A small number of non-DAergic neurons within the medial ZI projected to the lumbar spinal cord. We then characterized the DA A13 cells and report that these cells differ from canonical DA neurons since they lack the Dopamine Transporter (DAT). The lack of DAT expression, and possibly the lack of a dopamine reuptake mechanism, points to a longer time of action compared to typical dopamine neurons. Collectively our data suggest a parallel descending DAergic pathway from the A13 neurons of the medial ZI to the MLR, which we expect is important for modulating movement.

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Circuits controlling vertebrate locomotion: moving in a new direction.

Martyn Goulding (2009)

Neurobiologists have long sought to understand how circuits in the nervous system are organized to generate the precise neural outputs that underlie particular behaviours. The motor circuits in the spinal cord that control locomotion, commonly referred to as central pattern generator networks, provide an experimentally tractable model system for investigating how moderately complex ensembles of neurons generate select motor behaviours. The advent of novel molecular and genetic techniques coupled with recent advances in our knowledge of spinal cord development means that a comprehensive understanding of how the motor circuitry is organized and operates may be within our grasp.

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Midbrain circuits that set locomotor speed and gait selection

V. Caggiano, R Leiras, H. Goñi-Erro … (2018)

Summary Locomotion is a fundamental motor function common to the animal kingdom. It is executed episodically and adapted to behavioural needs including exploration, requiring slow locomotion, and escaping behaviour, necessitating faster speeds. The control of these functions originates in brainstem structures although the neuronal substrate(s) supporting them are debated. Here, we show in mice that speed/gait selection are controlled by glutamatergic excitatory neurons (GlutNs) segregated in two distinct midbrain nuclei: the Cuneiform Nucleus (CnF) and the Pedunculopontine Nucleus (PPN). GlutNs in each of those two regions are sufficient for controlling slower alternating locomotor behavior but only GlutNs in the CnF are necessary for high-speed synchronous locomotion. Additionally, PPN- and CnF-GlutNs activation dynamics and their input and output connectivity matrices support explorative and escape locomotion, respectively. Our results identify dual regions in the midbrain that act in common to select context dependent locomotor behaviours.

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Cell-Type-Specific Control of Brainstem Locomotor Circuits by Basal Ganglia.

Thomas K. Roseberry, A Lee, Arnaud L Lalive … (2016)

The basal ganglia (BG) are critical for adaptive motor control, but the circuit principles underlying their pathway-specific modulation of target regions are not well understood. Here, we dissect the mechanisms underlying BG direct and indirect pathway-mediated control of the mesencephalic locomotor region (MLR), a brainstem target of BG that is critical for locomotion. We optogenetically dissect the locomotor function of the three neurochemically distinct cell types within the MLR: glutamatergic, GABAergic, and cholinergic neurons. We find that the glutamatergic subpopulation encodes locomotor state and speed, is necessary and sufficient for locomotion, and is selectively innervated by BG. We further show activation and suppression, respectively, of MLR glutamatergic neurons by direct and indirect pathways, which is required for bidirectional control of locomotion by BG circuits. These findings provide a fundamental understanding of how BG can initiate or suppress a motor program through cell-type-specific regulation of neurons linked to specific actions.

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Author and article information

Contributors

Patrick J. Whelan:

ORCID: http://orcid.org/0000-0002-1234-5415

whelan@ucalgary.ca

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 22 May 2018

Publication date PMC-release: 22 May 2018

Publication date Collection: 2018

Volume: 8

Electronic Location Identifier: 7972

Affiliations

[1 ]ISNI 0000 0004 1936 7697, GRID grid.22072.35, Hotchkiss Brain Institute, , University of Calgary, ; Calgary, AB T2N 4N1 Canada

[2 ]ISNI 0000 0004 1936 7697, GRID grid.22072.35, Department of Comparative Biology and Experimental Medicine, , University of Calgary, ; Calgary, AB T2N 4N1 Canada

[3 ]ISNI 0000 0004 1936 7697, GRID grid.22072.35, Hotchkiss Brain Institute Advanced Microscopy Platform, , University of Calgary, ; Calgary, AB T2N 4N1 Canada

Author information

Sandeep Sharma http://orcid.org/0000-0003-4843-4951

Linda H. Kim http://orcid.org/0000-0003-0628-3104

Patrick J. Whelan http://orcid.org/0000-0002-1234-5415

Article

Publisher ID: 25908

DOI: 10.1038/s41598-018-25908-5

PMC ID: 5964077

PubMed ID: 29789702

SO-VID: 1a7eca95-798e-4a4c-a5d0-77161fd7ab06

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 21 September 2017

Date accepted : 30 April 2018

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