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      Activation of Brainstem Neurons During Mesencephalic Locomotor Region-Evoked Locomotion in the Cat

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          Abstract

          The distribution of locomotor-activated neurons in the brainstem of the cat was studied by c- Fos immunohistochemistry in combination with antibody-based cellular phenotyping following electrical stimulation of the mesencephalic locomotor region (MLR) – the anatomical constituents of which remain debated today, primarily between the cuneiform (CnF) and the pedunculopontine tegmental nuclei (PPT). Effective MLR sites were co-extensive with the CnF nucleus. Animals subject to the locomotor task showed abundant Fos labeling in the CnF, parabrachial nuclei of the subcuneiform region, periaqueductal gray, locus ceruleus (LC)/subceruleus (SubC), Kölliker–Fuse, magnocellular and lateral tegmental fields, raphe, and the parapyramidal region. Labeled neurons were more abundant on the side of stimulation. In some animals, Fos-labeled cells were also observed in the ventral tegmental area, medial and intermediate vestibular nuclei, dorsal motor nucleus of the vagus, n. tractus solitarii, and retrofacial nucleus in the ventrolateral medulla. Many neurons in the reticular formation were innervated by serotonergic fibers. Numerous locomotor-activated neurons in the parabrachial nuclei and LC/SubC/Kölliker–Fuse were noradrenergic. Few cholinergic neurons within the PPT stained for Fos. In the medulla, serotonergic neurons within the parapyramidal region and the nucleus raphe magnus were positive for Fos. Control animals, not subject to locomotion, showed few Fos-labeled neurons in these areas. The current study provides positive evidence for a role for the CnF in the initiation of locomotion while providing little evidence for the participation of the PPT. The results also show that MLR-evoked locomotion involves the parallel activation of reticular and monoaminergic neurons in the pons/medulla, and provides the anatomical and functional basis for spinal monoamine release during evoked locomotion. Lastly, the results indicate that vestibular, cardiovascular, and respiratory centers are centrally activated during MLR-evoked locomotion. Altogether, the results show a complex pattern of neuromodulatory influences of brainstem neurons by electrical activation of the MLR.

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          Neurophysiology of gait: from the spinal cord to the frontal lobe.

          Locomotion is a purposeful, goal-directed behavior initiated by signals arising from either volitional processing in the cerebral cortex or emotional processing in the limbic system. Regardless of whether the locomotion initiation is volitional or emotional, locomotion is accompanied by automatic controlled movement processes, such as the adjustment of postural muscle tone and rhythmic limb movements. Sensori-motor integration in the brainstem and the spinal cord plays crucial roles in this process. The basic locomotor motor pattern is generated by spinal interneuronal networks, termed central pattern generators (CPGs). Responding to signals in proprioceptive and skin afferents, the spinal interneuronal networks modify the locomotor pattern in cooperation with descending signals from the brainstem structures and the cerebral cortex. Information processing between the basal ganglia, the cerebellum, and the brainstem may enable automatic regulation of muscle tone and rhythmic limb movements in the absence of conscious awareness. However, when a locomoting subject encounters obstacles, the subject has to intentionally adjust bodily alignment to guide limb movements. Such an intentional gait modification requires motor programming in the premotor cortices. The motor programs utilize one's bodily information, such as the body schema, which is preserved and updated in the temporoparietal cortex. The motor programs are transmitted to the brainstem by the corticoreticulospinal system, so that one's posture is anticipatorily controlled. These processes enable the corticospinal system to generate limb trajectory and achieve accurate foot placement. Loops from the motor cortical areas to the basal ganglia and the cerebellum can serve this purpose. © 2013 Movement Disorder Society.
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            Midbrain circuits that set locomotor speed and gait selection

            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.

              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
                Journal
                Front Syst Neurosci
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Media S.A.
                1662-5137
                14 November 2019
                2019
                : 13
                : 69
                Affiliations
                [1] 1The Miami Project to Cure Paralysis, Department of Neurological Surgery, University of Miami Miller School of Medicine , Miami, FL, United States
                [2] 2Department of Physiology, Spinal Cord Research Centre, University of Manitoba , Winnipeg, MB, Canada
                Author notes

                Edited by: James W. Grau, Texas A&M University, United States

                Reviewed by: David Magnuson, University of Louisville, United States; Simon Arthur Sharples, University of St Andrews, United Kingdom

                *Correspondence: Brian R. Noga, bnoga@ 123456miami.edu

                Present address: Dawn M. G. Johnson, National Institute of Mental Health, Bethesda, MD, United States Songtao Xie, Department of Chemical and Natural Gas Engineering, Texas A&M University – Kingsville, Kingsville, TX, United States

                Article
                10.3389/fnsys.2019.00069
                6868058
                31798423
                451b65df-179a-4009-b5c8-8179323ee2f4
                Copyright © 2019 Opris, Dai, Johnson, Sanchez, Villamil, Xie, Lee-Hauser, Chang, Jordan and Noga.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 23 July 2019
                : 31 October 2019
                Page count
                Figures: 13, Tables: 1, Equations: 0, References: 177, Pages: 25, Words: 0
                Funding
                Funded by: Foundation for the National Institutes of Health 10.13039/100000009
                Award ID: RO1 NS046404
                Categories
                Neuroscience
                Original Research

                Neurosciences
                mesencephalic locomotor region,cuneiform nucleus,pedunculopontine nucleus,fictive locomotion,reticulospinal,monoamine,choline acetyltransferase,activity-dependent labeling

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