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Left-right side-specific neuropeptide mechanism mediates contralateral responses to a unilateral brain injury

Watanabe, Hiroyuki LU ; Nosova, Olga ; Sarkisyan, Daniil ; Andersen, Marlene Storm ; Carvalho, Liliana ; Galatenko, Vladimir ; Bazov, Igor ; Lukoyanov, Nikolay ; Maia, Gisela H. and Hallberg, Mathias , et al. (2021) In eNeuro 8(3).
Abstract

Neuropeptides are implicated in control of lateralized processes in the brain. A unilateral brain injury (UBI) causes the contralesional sensorimotor deficits. To examine whether opioid neuropeptides mediate UBI induced asymmetric processes we compared effects of opioid antagonists on the contralesional and ipsile-sional hindlimb responses to the left-sided and right-sided injury in rats. UBI induced hindlimb postural asymmetry (HL-PA) with the contralesional hindlimb flexion, and activated contralesional withdrawal reflex of extensor digitorum longus (EDL) evoked by electrical stimulation and recorded with EMG technique. No effects on the interossei (Int) and peroneaus longus (PL) were evident. The general opioid antagonist naloxone... (More)

Neuropeptides are implicated in control of lateralized processes in the brain. A unilateral brain injury (UBI) causes the contralesional sensorimotor deficits. To examine whether opioid neuropeptides mediate UBI induced asymmetric processes we compared effects of opioid antagonists on the contralesional and ipsile-sional hindlimb responses to the left-sided and right-sided injury in rats. UBI induced hindlimb postural asymmetry (HL-PA) with the contralesional hindlimb flexion, and activated contralesional withdrawal reflex of extensor digitorum longus (EDL) evoked by electrical stimulation and recorded with EMG technique. No effects on the interossei (Int) and peroneaus longus (PL) were evident. The general opioid antagonist naloxone blocked postural effects, did not change EDL asymmetry while uncovered cryptic asymmetry in the PL and Int reflexes induced by UBI. Thus, the spinal opioid system may either mediate or counteract the injury effects. Strikingly, effects of selective opioid antagonists were the injury side-specific. The *-antagonist β-funaltrex-amine (FNA) and κ-antagonist nor-binaltorphimine (BNI) reduced postural asymmetry after the right but not left UBI. In contrast, the δ-antagonist naltrindole (NTI) inhibited HL-PA after the left but not right-side brain injury. The opioid gene expression and opioid peptides were lateralized in the lumbar spinal cord, and coordination between expression of the opioid and neuroplasticity-related genes was impaired by UBI that together may underlie the side-specific effects of the antagonists. We suggest that mirror-symmetric neural circuits that mediate effects of left and right brain injury on the contralesional hindlimbs are differentially controlled by the lateralized opioid system.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Brain injury, Left-right side-specific regulation, Opioid system, Postural asymmetry, Withdrawal reflexes
in
eNeuro
volume
8
issue
3
article number
ENEURO.0548-20.2021
publisher
Society for Neuroscience
external identifiers
  • pmid:33903183
  • scopus:85105746412
ISSN
2373-2822
DOI
10.1523/ENEURO.0548-20.2021
language
English
LU publication?
yes
id
5ca5f067-2b78-4bdd-9b18-7e7dde4d50fe
date added to LUP
2022-03-09 17:02:47
date last changed
2024-03-21 06:14:02
@article{5ca5f067-2b78-4bdd-9b18-7e7dde4d50fe,
  abstract     = {{<p>Neuropeptides are implicated in control of lateralized processes in the brain. A unilateral brain injury (UBI) causes the contralesional sensorimotor deficits. To examine whether opioid neuropeptides mediate UBI induced asymmetric processes we compared effects of opioid antagonists on the contralesional and ipsile-sional hindlimb responses to the left-sided and right-sided injury in rats. UBI induced hindlimb postural asymmetry (HL-PA) with the contralesional hindlimb flexion, and activated contralesional withdrawal reflex of extensor digitorum longus (EDL) evoked by electrical stimulation and recorded with EMG technique. No effects on the interossei (Int) and peroneaus longus (PL) were evident. The general opioid antagonist naloxone blocked postural effects, did not change EDL asymmetry while uncovered cryptic asymmetry in the PL and Int reflexes induced by UBI. Thus, the spinal opioid system may either mediate or counteract the injury effects. Strikingly, effects of selective opioid antagonists were the injury side-specific. The *-antagonist β-funaltrex-amine (FNA) and κ-antagonist nor-binaltorphimine (BNI) reduced postural asymmetry after the right but not left UBI. In contrast, the δ-antagonist naltrindole (NTI) inhibited HL-PA after the left but not right-side brain injury. The opioid gene expression and opioid peptides were lateralized in the lumbar spinal cord, and coordination between expression of the opioid and neuroplasticity-related genes was impaired by UBI that together may underlie the side-specific effects of the antagonists. We suggest that mirror-symmetric neural circuits that mediate effects of left and right brain injury on the contralesional hindlimbs are differentially controlled by the lateralized opioid system.</p>}},
  author       = {{Watanabe, Hiroyuki and Nosova, Olga and Sarkisyan, Daniil and Andersen, Marlene Storm and Carvalho, Liliana and Galatenko, Vladimir and Bazov, Igor and Lukoyanov, Nikolay and Maia, Gisela H. and Hallberg, Mathias and Zhang, Mengliang and Schouenborg, Jens and Bakalkin, Georgy}},
  issn         = {{2373-2822}},
  keywords     = {{Brain injury; Left-right side-specific regulation; Opioid system; Postural asymmetry; Withdrawal reflexes}},
  language     = {{eng}},
  number       = {{3}},
  publisher    = {{Society for Neuroscience}},
  series       = {{eNeuro}},
  title        = {{Left-right side-specific neuropeptide mechanism mediates contralateral responses to a unilateral brain injury}},
  url          = {{http://dx.doi.org/10.1523/ENEURO.0548-20.2021}},
  doi          = {{10.1523/ENEURO.0548-20.2021}},
  volume       = {{8}},
  year         = {{2021}},
}