An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole

Vertebrate locomotion is heavily dependent on descending control originating in the midbrain and subsequently influencing central pattern generators in the spinal cord. However, the midbrain neuronal circuitry and its connections with other brainstem and spinal motor circuits has not been fully eluc...

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Main Authors: Michelle Christine Larbi, Giulia Messa, Helin Jalal, Stella Koutsikou
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncir.2022.1027831/full
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author Michelle Christine Larbi
Giulia Messa
Helin Jalal
Stella Koutsikou
author_facet Michelle Christine Larbi
Giulia Messa
Helin Jalal
Stella Koutsikou
author_sort Michelle Christine Larbi
collection DOAJ
description Vertebrate locomotion is heavily dependent on descending control originating in the midbrain and subsequently influencing central pattern generators in the spinal cord. However, the midbrain neuronal circuitry and its connections with other brainstem and spinal motor circuits has not been fully elucidated. Vertebrates with very simple nervous system, like the hatchling Xenopus laevis tadpole, have been instrumental in unravelling fundamental principles of locomotion and its suspraspinal control. Here, we use behavioral and electrophysiological approaches in combination with lesions of the midbrain to investigate its contribution to the initiation and control of the tadpole swimming in response to trunk skin stimulation. None of the midbrain lesions studied here blocked the tadpole’s sustained swim behavior following trunk skin stimulation. However, we identified that distinct midbrain lesions led to significant changes in the latency and trajectory of swimming. These changes could partly be explained by the increase in synchronous muscle contractions on the opposite sides of the tadpole’s body and permanent deflection of the tail from its normal position, respectively. We conclude that the tadpole’s embryonic trunk skin sensorimotor pathway involves the midbrain, which harbors essential neuronal circuitry to significantly contribute to the appropriate, timely and coordinated selection and execution of locomotion, imperative to the animal’s survival.
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spelling doaj.art-383e6287625d4f31ad0454c12d1124242022-12-22T04:24:19ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102022-12-011610.3389/fncir.2022.10278311027831An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpoleMichelle Christine LarbiGiulia MessaHelin JalalStella KoutsikouVertebrate locomotion is heavily dependent on descending control originating in the midbrain and subsequently influencing central pattern generators in the spinal cord. However, the midbrain neuronal circuitry and its connections with other brainstem and spinal motor circuits has not been fully elucidated. Vertebrates with very simple nervous system, like the hatchling Xenopus laevis tadpole, have been instrumental in unravelling fundamental principles of locomotion and its suspraspinal control. Here, we use behavioral and electrophysiological approaches in combination with lesions of the midbrain to investigate its contribution to the initiation and control of the tadpole swimming in response to trunk skin stimulation. None of the midbrain lesions studied here blocked the tadpole’s sustained swim behavior following trunk skin stimulation. However, we identified that distinct midbrain lesions led to significant changes in the latency and trajectory of swimming. These changes could partly be explained by the increase in synchronous muscle contractions on the opposite sides of the tadpole’s body and permanent deflection of the tail from its normal position, respectively. We conclude that the tadpole’s embryonic trunk skin sensorimotor pathway involves the midbrain, which harbors essential neuronal circuitry to significantly contribute to the appropriate, timely and coordinated selection and execution of locomotion, imperative to the animal’s survival.https://www.frontiersin.org/articles/10.3389/fncir.2022.1027831/fullmidbrainlocomotionswimmingXenopusdescending controlbrainstem
spellingShingle Michelle Christine Larbi
Giulia Messa
Helin Jalal
Stella Koutsikou
An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole
Frontiers in Neural Circuits
midbrain
locomotion
swimming
Xenopus
descending control
brainstem
title An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole
title_full An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole
title_fullStr An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole
title_full_unstemmed An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole
title_short An early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole
title_sort early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling xenopus laevis tadpole
topic midbrain
locomotion
swimming
Xenopus
descending control
brainstem
url https://www.frontiersin.org/articles/10.3389/fncir.2022.1027831/full
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