Frontal and frontoparietal injury differentially affect the ipsilateral corticospinal projection from the nonlesioned hemisphere in monkey (Macaca mulatta)

J Comp Neurol. 2016 Feb 1;524(2):380-407. doi: 10.1002/cne.23861. Epub 2015 Aug 18.

Abstract

Upper extremity hemiplegia is a common consequence of unilateral cortical stroke. Understanding the role of the unaffected cerebral hemisphere in the motor recovery process has been encouraged, in part, by the presence of ipsilateral corticospinal projections (iCSP). We examined the neuroplastic response of the iCSP from the contralesional primary motor cortex (cM1) hand/arm area to spinal levels C5-T1 after spontaneous long-term recovery from isolated frontal lobe injury and isolated frontoparietal injury. High-resolution tract tracing, stereological, and behavioral methodologies were applied. Recovery from frontal motor injury resulted in enhanced numbers of terminal labeled boutons in the iCSP from cM1 compared with controls. Increases occurred in lamina VIII and the adjacent ventral sectors of lamina VII, which are involved in axial/proximal limb sensorimotor processing. Larger frontal lobe lesions were associated with greater numbers of terminal boutons than smaller frontal lobe lesions. In contrast, frontoparietal injury blocked this response; total bouton number was similar to controls, demonstrating that disruption of somatosensory input to one hemisphere has a suppressive effect on the iCSP from the nonlesioned hemisphere. However, compared with controls, elevated bouton numbers occurred in lamina VIII, at the expense of lamina VII bouton labeling. Lamina IX boutons were also elevated in two frontoparietal lesion cases with extensive cortical injury. Because laminae VIII and IX collectively harbor axial, proximal, and distal motoneurons, therapeutic intervention targeting the ipsilateral corticospinal linkage from cM1 may promote proximal, and possibly distal, upper-limb motor recovery following frontal and frontoparietal injury.

Keywords: corticofugal; frontal lobe; hand movements; motor recovery; neurosurgical resection; parietal lobe; plasticity; pyramidal tract; spinal cord.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain Injuries / pathology*
  • Brain Injuries / physiopathology*
  • Disease Models, Animal
  • Frontal Lobe / pathology*
  • Functional Laterality / physiology*
  • Isoquinolines / metabolism
  • Macaca mulatta
  • Microinjections
  • Parietal Lobe / pathology*
  • Pyramidal Tracts / pathology
  • Pyramidal Tracts / physiopathology*

Substances

  • Isoquinolines
  • lucifer yellow