Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury

Brain injuries can interrupt descending neural pathways that convey motor commands from the cortex to spinal motoneurons. Here, we demonstrate that a unilateral injury of the hindlimb sensorimotor cortex of rats with completely transected thoracic spinal cord produces hindlimb postural asymmetry wit...

Full description

Bibliographic Details
Main Authors: Nikolay Lukoyanov, Hiroyuki Watanabe, Liliana S Carvalho, Olga Kononenko, Daniil Sarkisyan, Mengliang Zhang, Marlene Storm Andersen, Elena A Lukoyanova, Vladimir Galatenko, Alex Tonevitsky, Igor Bazov, Tatiana Iakovleva, Jens Schouenborg, Georgy Bakalkin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/65247
id doaj-47663e8d250242919e735760ac862479
record_format Article
spelling doaj-47663e8d250242919e735760ac8624792021-08-10T07:00:41ZengeLife Sciences Publications LtdeLife2050-084X2021-08-011010.7554/eLife.65247Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injuryNikolay Lukoyanov0Hiroyuki Watanabe1Liliana S Carvalho2Olga Kononenko3https://orcid.org/0000-0002-1332-7067Daniil Sarkisyan4Mengliang Zhang5Marlene Storm Andersen6Elena A Lukoyanova7Vladimir Galatenko8Alex Tonevitsky9Igor Bazov10https://orcid.org/0000-0003-4388-1656Tatiana Iakovleva11Jens Schouenborg12Georgy Bakalkin13https://orcid.org/0000-0002-8074-9833Departamento de Biomedicina da Faculdade de Medicina da Universidade do Porto, Instituto de Investigação e Inovação em Saúde, Instituto de Biologia Molecular e Celular, Porto, PortugalDepartment of Pharmaceutical Biosciences, Uppsala University, Uppsala, SwedenDepartamento de Biomedicina da Faculdade de Medicina da Universidade do Porto, Instituto de Investigação e Inovação em Saúde, Instituto de Biologia Molecular e Celular, Porto, PortugalDepartment of Pharmaceutical Biosciences, Uppsala University, Uppsala, SwedenDepartment of Pharmaceutical Biosciences, Uppsala University, Uppsala, SwedenNeuronano Research Center, Department of Experimental Medical Science, Lund University, Lund, Sweden; Department of Molecular Medicine, University of Southern Denmark, Odense, DenmarkDepartment of Molecular Medicine, University of Southern Denmark, Odense, DenmarkDepartamento de Biomedicina da Faculdade de Medicina da Universidade do Porto, Instituto de Investigação e Inovação em Saúde, Instituto de Biologia Molecular e Celular, Porto, PortugalFaculty of Mechanics and Mathematics, Lomonosov Moscow State University, Moscow, Russian FederationFaculty of Biology and Biotechnology, National Research University Higher School of Economics, Moscow, Russian Federation; Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry RAS, Moscow, Russian FederationDepartment of Pharmaceutical Biosciences, Uppsala University, Uppsala, SwedenDepartment of Pharmaceutical Biosciences, Uppsala University, Uppsala, SwedenNeuronano Research Center, Department of Experimental Medical Science, Lund University, Lund, SwedenDepartment of Pharmaceutical Biosciences, Uppsala University, Uppsala, SwedenBrain injuries can interrupt descending neural pathways that convey motor commands from the cortex to spinal motoneurons. Here, we demonstrate that a unilateral injury of the hindlimb sensorimotor cortex of rats with completely transected thoracic spinal cord produces hindlimb postural asymmetry with contralateral flexion and asymmetric hindlimb withdrawal reflexes within 3 hr, as well as asymmetry in gene expression patterns in the lumbar spinal cord. The injury-induced postural effects were abolished by hypophysectomy and were mimicked by transfusion of serum from animals with brain injury. Administration of the pituitary neurohormones β-endorphin or Arg-vasopressin-induced side-specific hindlimb responses in naive animals, while antagonists of the opioid and vasopressin receptors blocked hindlimb postural asymmetry in rats with brain injury. Thus, in addition to the well-established involvement of motor pathways descending from the brain to spinal circuits, the side-specific humoral signaling may also add to postural and reflex asymmetries seen after brain injury.https://elifesciences.org/articles/65247neuroendocrine signalingbrain injuryneurohormonespostural asymmetrynociceptive withdrawal reflexleft-right side
collection DOAJ
language English
format Article
sources DOAJ
author Nikolay Lukoyanov
Hiroyuki Watanabe
Liliana S Carvalho
Olga Kononenko
Daniil Sarkisyan
Mengliang Zhang
Marlene Storm Andersen
Elena A Lukoyanova
Vladimir Galatenko
Alex Tonevitsky
Igor Bazov
Tatiana Iakovleva
Jens Schouenborg
Georgy Bakalkin
spellingShingle Nikolay Lukoyanov
Hiroyuki Watanabe
Liliana S Carvalho
Olga Kononenko
Daniil Sarkisyan
Mengliang Zhang
Marlene Storm Andersen
Elena A Lukoyanova
Vladimir Galatenko
Alex Tonevitsky
Igor Bazov
Tatiana Iakovleva
Jens Schouenborg
Georgy Bakalkin
Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury
eLife
neuroendocrine signaling
brain injury
neurohormones
postural asymmetry
nociceptive withdrawal reflex
left-right side
author_facet Nikolay Lukoyanov
Hiroyuki Watanabe
Liliana S Carvalho
Olga Kononenko
Daniil Sarkisyan
Mengliang Zhang
Marlene Storm Andersen
Elena A Lukoyanova
Vladimir Galatenko
Alex Tonevitsky
Igor Bazov
Tatiana Iakovleva
Jens Schouenborg
Georgy Bakalkin
author_sort Nikolay Lukoyanov
title Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury
title_short Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury
title_full Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury
title_fullStr Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury
title_full_unstemmed Left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury
title_sort left-right side-specific endocrine signaling complements neural pathways to mediate acute asymmetric effects of brain injury
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-08-01
description Brain injuries can interrupt descending neural pathways that convey motor commands from the cortex to spinal motoneurons. Here, we demonstrate that a unilateral injury of the hindlimb sensorimotor cortex of rats with completely transected thoracic spinal cord produces hindlimb postural asymmetry with contralateral flexion and asymmetric hindlimb withdrawal reflexes within 3 hr, as well as asymmetry in gene expression patterns in the lumbar spinal cord. The injury-induced postural effects were abolished by hypophysectomy and were mimicked by transfusion of serum from animals with brain injury. Administration of the pituitary neurohormones β-endorphin or Arg-vasopressin-induced side-specific hindlimb responses in naive animals, while antagonists of the opioid and vasopressin receptors blocked hindlimb postural asymmetry in rats with brain injury. Thus, in addition to the well-established involvement of motor pathways descending from the brain to spinal circuits, the side-specific humoral signaling may also add to postural and reflex asymmetries seen after brain injury.
topic neuroendocrine signaling
brain injury
neurohormones
postural asymmetry
nociceptive withdrawal reflex
left-right side
url https://elifesciences.org/articles/65247
work_keys_str_mv AT nikolaylukoyanov leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT hiroyukiwatanabe leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT lilianascarvalho leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT olgakononenko leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT daniilsarkisyan leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT mengliangzhang leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT marlenestormandersen leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT elenaalukoyanova leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT vladimirgalatenko leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT alextonevitsky leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT igorbazov leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT tatianaiakovleva leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT jensschouenborg leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
AT georgybakalkin leftrightsidespecificendocrinesignalingcomplementsneuralpathwaystomediateacuteasymmetriceffectsofbraininjury
_version_ 1721212663476781056