Circuits for State-Dependent Modulation of Locomotion

Autores
Pernía Andrade, Alejandro J.; Wenger, Nikolaus; Esposito, Maria Soledad; Tovote, Philip
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Pernía Andrade, Alejandro J.. University Hospital Würzburg; Alemania
Fil: Wenger, Nikolaus. Humboldt-Universität zu Berlin; Alemania. Freie Universität Berlin; Alemania
Fil: Esposito, Maria Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte; Argentina. Comisión Nacional de Energía Atómica. Centro Atómico Bariloche; Argentina
Fil: Tovote, Philip. Universität Würzburg; Alemania. University Hospital Würzburg; Alemania
Materia
CIRCUITS AND CIRCUIT COMPONENTS
EMOTIONAL STATES
GAIT
LOCOMOTION
MOTOR CONTROL
NEURAL NETWORKS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/167632

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network_name_str CONICET Digital (CONICET)
spelling Circuits for State-Dependent Modulation of LocomotionPernía Andrade, Alejandro J.Wenger, NikolausEsposito, Maria SoledadTovote, PhilipCIRCUITS AND CIRCUIT COMPONENTSEMOTIONAL STATESGAITLOCOMOTIONMOTOR CONTROLNEURAL NETWORKShttps://purl.org/becyt/ford/3.5https://purl.org/becyt/ford/3Brain-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.Fil: Pernía Andrade, Alejandro J.. University Hospital Würzburg; AlemaniaFil: Wenger, Nikolaus. Humboldt-Universität zu Berlin; Alemania. Freie Universität Berlin; AlemaniaFil: Esposito, Maria Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte; Argentina. Comisión Nacional de Energía Atómica. Centro Atómico Bariloche; ArgentinaFil: Tovote, Philip. Universität Würzburg; Alemania. University Hospital Würzburg; AlemaniaFrontiers Media2021-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/167632Pernía Andrade, Alejandro J.; Wenger, Nikolaus; Esposito, Maria Soledad; Tovote, Philip; Circuits for State-Dependent Modulation of Locomotion; Frontiers Media; Frontiers In Human Neuroscience; 15; 745689; 11-2021; 1-201662-5161CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.3389/fnhum.2021.745689info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fnhum.2021.745689/fullinfo:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:24:49Zoai:ri.conicet.gov.ar:11336/167632instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-15 14:24:49.766CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Circuits for State-Dependent Modulation of Locomotion
title Circuits for State-Dependent Modulation of Locomotion
spellingShingle Circuits for State-Dependent Modulation of Locomotion
Pernía Andrade, Alejandro J.
CIRCUITS AND CIRCUIT COMPONENTS
EMOTIONAL STATES
GAIT
LOCOMOTION
MOTOR CONTROL
NEURAL NETWORKS
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
dc.creator.none.fl_str_mv Pernía Andrade, Alejandro J.
Wenger, Nikolaus
Esposito, Maria Soledad
Tovote, Philip
author Pernía Andrade, Alejandro J.
author_facet Pernía Andrade, Alejandro J.
Wenger, Nikolaus
Esposito, Maria Soledad
Tovote, Philip
author_role author
author2 Wenger, Nikolaus
Esposito, Maria Soledad
Tovote, Philip
author2_role author
author
author
dc.subject.none.fl_str_mv CIRCUITS AND CIRCUIT COMPONENTS
EMOTIONAL STATES
GAIT
LOCOMOTION
MOTOR CONTROL
NEURAL NETWORKS
topic CIRCUITS AND CIRCUIT COMPONENTS
EMOTIONAL STATES
GAIT
LOCOMOTION
MOTOR CONTROL
NEURAL NETWORKS
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.5
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv 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.
Fil: Pernía Andrade, Alejandro J.. University Hospital Würzburg; Alemania
Fil: Wenger, Nikolaus. Humboldt-Universität zu Berlin; Alemania. Freie Universität Berlin; Alemania
Fil: Esposito, Maria Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte; Argentina. Comisión Nacional de Energía Atómica. Centro Atómico Bariloche; Argentina
Fil: Tovote, Philip. Universität Würzburg; Alemania. University Hospital Würzburg; Alemania
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.
publishDate 2021
dc.date.none.fl_str_mv 2021-11
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/167632
Pernía Andrade, Alejandro J.; Wenger, Nikolaus; Esposito, Maria Soledad; Tovote, Philip; Circuits for State-Dependent Modulation of Locomotion; Frontiers Media; Frontiers In Human Neuroscience; 15; 745689; 11-2021; 1-20
1662-5161
CONICET Digital
CONICET
url http://hdl.handle.net/11336/167632
identifier_str_mv Pernía Andrade, Alejandro J.; Wenger, Nikolaus; Esposito, Maria Soledad; Tovote, Philip; Circuits for State-Dependent Modulation of Locomotion; Frontiers Media; Frontiers In Human Neuroscience; 15; 745689; 11-2021; 1-20
1662-5161
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fnhum.2021.745689/full
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
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dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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