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Research Articles, Neurobiology of Disease

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 and Randolph J. Nudo
Journal of Neuroscience 15 March 2023, 43 (11) 2021-2032; DOI: https://doi.org/10.1523/JNEUROSCI.1452-22.2023
Erik J. Plautz
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
2Landon Center on Aging, University of Kansas Medical Center, Kansas City, Kansas 66160
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Scott Barbay
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
2Landon Center on Aging, University of Kansas Medical Center, Kansas City, Kansas 66160
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  • ORCID record for Scott Barbay
Shawn B. Frost
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
2Landon Center on Aging, University of Kansas Medical Center, Kansas City, Kansas 66160
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Ann M. Stowe
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
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Numa Dancause
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
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Elena V. Zoubina
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
2Landon Center on Aging, University of Kansas Medical Center, Kansas City, Kansas 66160
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Ines Eisner-Janowicz
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
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David J. Guggenmos
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
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Randolph J. Nudo
1Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160
2Landon Center on Aging, University of Kansas Medical Center, Kansas City, Kansas 66160
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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 (+110.6%) 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.

SIGNIFICANCE STATEMENT The relationship between motor recovery and motor map reorganization after cortical injury has rarely been examined in acute/subacute periods. In nonhuman primates, premotor maps were examined at 2 and 3 weeks after injury to primary motor cortex. Although maps are known to expand late after injury, the present study demonstrates early map expansion at 2 weeks (dorsal premotor cortex) followed by contraction at 3 weeks (dorsal and ventral premotor cortex). This nonlinear map reorganization during a time of gradual behavioral recovery suggests that the relationship between map plasticity and motor recovery is much more complex than previously thought. It also suggests that rehabilitative motor training may have its most potent effects during this early dynamic phase of map reorganization.

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

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The Journal of Neuroscience: 43 (11)
Journal of Neuroscience
Vol. 43, Issue 11
15 Mar 2023
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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
Journal of Neuroscience 15 March 2023, 43 (11) 2021-2032; DOI: 10.1523/JNEUROSCI.1452-22.2023

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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
Journal of Neuroscience 15 March 2023, 43 (11) 2021-2032; DOI: 10.1523/JNEUROSCI.1452-22.2023
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Keywords

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

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