Circuits for State-Dependent Modulation of Locomotion

Brain-wide neural circuits enable bi- and quadrupeds to express adaptive locomotor behaviors in a context- and state-dependent manner, e.g., in response to threats or rewards. These behaviors include dynamic transitions between initiation, maintenance and termination of locomotion. Advances within t...

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Autores principales:	Alejandro J. Pernía-Andrade, Nikolaus Wenger, Maria S. Esposito, Philip Tovote
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	circuits and circuit components motor control neural networks gait emotional states locomotion Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
Acceso en línea:	https://doaj.org/article/8eebed92b0ed42f5a07d712b8e1b7d29
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spelling	oai:doaj.org-article:8eebed92b0ed42f5a07d712b8e1b7d292021-11-10T06:26:23ZCircuits for State-Dependent Modulation of Locomotion1662-516110.3389/fnhum.2021.745689https://doaj.org/article/8eebed92b0ed42f5a07d712b8e1b7d292021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fnhum.2021.745689/fullhttps://doaj.org/toc/1662-5161Brain-wide neural circuits enable bi- and quadrupeds to express adaptive locomotor behaviors in a context- and state-dependent manner, e.g., in response to threats or rewards. These behaviors include dynamic transitions between initiation, maintenance and termination of locomotion. Advances within the last decade have revealed an intricate coordination of these individual locomotion phases by complex interaction of multiple brain circuits. This review provides an overview of the neural basis of state-dependent modulation of locomotion initiation, maintenance and termination, with a focus on insights from circuit-centered studies in rodents. The reviewed evidence indicates that a brain-wide network involving excitatory circuit elements connecting cortex, midbrain and medullary areas appears to be the common substrate for the initiation of locomotion across different higher-order states. Specific network elements within motor cortex and the mesencephalic locomotor region drive the initial postural adjustment and the initiation of locomotion. Microcircuits of the basal ganglia, by implementing action-selection computations, trigger goal-directed locomotion. The initiation of locomotion is regulated by neuromodulatory circuits residing in the basal forebrain, the hypothalamus, and medullary regions such as locus coeruleus. The maintenance of locomotion requires the interaction of an even larger neuronal network involving motor, sensory and associative cortical elements, as well as defined circuits within the superior colliculus, the cerebellum, the periaqueductal gray, the mesencephalic locomotor region and the medullary reticular formation. Finally, locomotor arrest as an important component of defensive emotional states, such as acute anxiety, is mediated via a network of survival circuits involving hypothalamus, amygdala, periaqueductal gray and medullary premotor centers. By moving beyond the organizational principle of functional brain regions, this review promotes a circuit-centered perspective of locomotor regulation by higher-order states, and emphasizes the importance of individual network elements such as cell types and projection pathways. The realization that dysfunction within smaller, identifiable circuit elements can affect the larger network function supports more mechanistic and targeted therapeutic intervention in the treatment of motor network disorders.Alejandro J. Pernía-AndradeNikolaus WengerMaria S. EspositoPhilip TovotePhilip TovoteFrontiers Media S.A.articlecircuits and circuit componentsmotor controlneural networksgaitemotional stateslocomotionNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENFrontiers in Human Neuroscience, Vol 15 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	circuits and circuit components motor control neural networks gait emotional states locomotion Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
spellingShingle	circuits and circuit components motor control neural networks gait emotional states locomotion Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Alejandro J. Pernía-Andrade Nikolaus Wenger Maria S. Esposito Philip Tovote Philip Tovote Circuits for State-Dependent Modulation of Locomotion
description	Brain-wide neural circuits enable bi- and quadrupeds to express adaptive locomotor behaviors in a context- and state-dependent manner, e.g., in response to threats or rewards. These behaviors include dynamic transitions between initiation, maintenance and termination of locomotion. Advances within the last decade have revealed an intricate coordination of these individual locomotion phases by complex interaction of multiple brain circuits. This review provides an overview of the neural basis of state-dependent modulation of locomotion initiation, maintenance and termination, with a focus on insights from circuit-centered studies in rodents. The reviewed evidence indicates that a brain-wide network involving excitatory circuit elements connecting cortex, midbrain and medullary areas appears to be the common substrate for the initiation of locomotion across different higher-order states. Specific network elements within motor cortex and the mesencephalic locomotor region drive the initial postural adjustment and the initiation of locomotion. Microcircuits of the basal ganglia, by implementing action-selection computations, trigger goal-directed locomotion. The initiation of locomotion is regulated by neuromodulatory circuits residing in the basal forebrain, the hypothalamus, and medullary regions such as locus coeruleus. The maintenance of locomotion requires the interaction of an even larger neuronal network involving motor, sensory and associative cortical elements, as well as defined circuits within the superior colliculus, the cerebellum, the periaqueductal gray, the mesencephalic locomotor region and the medullary reticular formation. Finally, locomotor arrest as an important component of defensive emotional states, such as acute anxiety, is mediated via a network of survival circuits involving hypothalamus, amygdala, periaqueductal gray and medullary premotor centers. By moving beyond the organizational principle of functional brain regions, this review promotes a circuit-centered perspective of locomotor regulation by higher-order states, and emphasizes the importance of individual network elements such as cell types and projection pathways. The realization that dysfunction within smaller, identifiable circuit elements can affect the larger network function supports more mechanistic and targeted therapeutic intervention in the treatment of motor network disorders.
format	article
author	Alejandro J. Pernía-Andrade Nikolaus Wenger Maria S. Esposito Philip Tovote Philip Tovote
author_facet	Alejandro J. Pernía-Andrade Nikolaus Wenger Maria S. Esposito Philip Tovote Philip Tovote
author_sort	Alejandro J. Pernía-Andrade
title	Circuits for State-Dependent Modulation of Locomotion
title_short	Circuits for State-Dependent Modulation of Locomotion
title_full	Circuits for State-Dependent Modulation of Locomotion
title_fullStr	Circuits for State-Dependent Modulation of Locomotion
title_full_unstemmed	Circuits for State-Dependent Modulation of Locomotion
title_sort	circuits for state-dependent modulation of locomotion
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/8eebed92b0ed42f5a07d712b8e1b7d29
work_keys_str_mv	AT alejandrojperniaandrade circuitsforstatedependentmodulationoflocomotion AT nikolauswenger circuitsforstatedependentmodulationoflocomotion AT mariasesposito circuitsforstatedependentmodulationoflocomotion AT philiptovote circuitsforstatedependentmodulationoflocomotion AT philiptovote circuitsforstatedependentmodulationoflocomotion
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Circuits for State-Dependent Modulation of Locomotion

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