Spared Premotor Areas Undergo Rapid Nonlinear Changes in Functional Organization following a Focal Ischemic Infarct in Primary Motor Cortex of Squirrel Monkeys

Erik J. Plautz, Scott Barbay, Shawn B. Frost, Ann M. Stowe, Numa Dancause, Elena V. Zoubina, Ines Eisner-Janowicz, David J. Guggenmos, Randolph J. Nudo

Research output: Contribution to journalArticlepeer-review

Abstract

Recovery of motor function after stroke is accompanied by reorganization of movement representations in spared cortical motor regions. It is widely assumed that map reorganization parallels recovery, suggesting a causal relationship. We examined this assumption by measuring changes in motor representations in eight male and six female squirrel monkeys in the first few weeks after injury, a time when motor recovery is most rapid. Maps of movement representations were derived using intracortical microstimulation techniques in primary motor cortex (M1), ventral premotor cortex (PMv), and dorsal premotor cortex (PMd) in 14 adult squirrel monkeys before and after a focal infarct in the M1 distal forelimb area. Maps were derived at baseline and at either 2 (n = 7) or 3 weeks (n = 7) postinfarct. In PMv the forelimb maps remained unchanged at 2 weeks but contracted significantly (-42.4%) at 3 weeks. In PMd the forelimb maps expanded significantly (1110.6%) at 2 weeks but contracted significantly (-57.4%) at 3 weeks. Motor deficits were equivalent at both time points. These results highlight two features of plasticity after M1 lesions. First, significant contraction of distal forelimb motor maps in both PMv and PMd is evident by 3 weeks. Second, an unpredictable nonlinear pattern of reorganization occurs in the distal forelimb representation in PMd, first expanding at 2 weeks, and then contracting at 3 weeks postinjury. Together with previous results demonstrating reliable map expansions in PMv several weeks to months after M1 injury, the subacute time period may represent a critical window for the timing of therapeutic interventions.

Original languageEnglish
Pages (from-to)2021-2032
Number of pages12
JournalJournal of Neuroscience
Volume43
Issue number11
DOIs
StatePublished - Mar 15 2023

Bibliographical note

Funding Information:
Received July 23, 2022; revised Jan. 10, 2023; accepted Jan. 13, 2023. Author contributions: E.J.P. and R.J.N. designed research; E.J.P., S.B., S.B.F., A.M.S., N.D., E.V.Z., I.E.-J., and D.J.G. performed research; E.J.P. and S.B. analyzed data; and E.P., S.B., and R.J.N. wrote the paper. This work was supported by National Institues of Health Grants U54 NS048126, NIH R01 NS30853, and P30 HD002528 and Northstar Neuroscience. We thank Bob Cross, Caleb Dunham, Erica Hoover, Diane Larson, and Phuong Nguyen for technical assistance and Scott Bury, Pei-chun Fang, David McNeal, Michael Taylor, and Ed Urban for assistance with collection of mapping data. The authors declare no competing financial interests. Correspondence should be sent to Randolph J. Nudo at rnudo@kumc.edu or Erik Plautz at erik.plautz@utsouthwestern.edu. https://doi.org/10.1523/JNEUROSCI.1452-22.2023 Copyright © 2023 the authors

Publisher Copyright:
Copyright © 2023 the authors.

Keywords

  • cortical plasticity
  • ICMS
  • motor maps
  • premotor cortex
  • recovery of function
  • stroke

ASJC Scopus subject areas

  • Neuroscience (all)

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