Selective long-term reorganization of the corticospinal projection from the supplementary motor cortex following recovery from lateral motor cortex injury

J Comp Neurol. 2010 Mar 1;518(5):586-621. doi: 10.1002/cne.22218.

Abstract

Brain injury affecting the frontal motor cortex or its descending axons often causes contralateral upper extremity paresis. Although recovery is variable, the underlying mechanisms supporting favorable motor recovery remain unclear. Because the medial wall of the cerebral hemisphere is often spared following brain injury and recent functional neuroimaging studies in patients indicate a potential role for this brain region in the recovery process, we investigated the long-term effects of isolated lateral frontal motor cortical injury on the corticospinal projection (CSP) from intact, ipsilesional supplementary motor cortex (M2). After injury to the arm region of the primary motor (M1) and lateral premotor (LPMC) cortices, upper extremity recovery is accompanied by terminal axon plasticity in the contralateral CSP but not the ipsilateral CSP from M2. Furthermore, significant contralateral plasticity occurs only in lamina VII and dorsally within lamina IX. Thus, selective intraspinal sprouting transpires in regions containing interneurons, flexor-related motor neurons, and motor neurons supplying intrinsic hand muscles, which all play important roles in mediating reaching and digit movements. After recovery, subsequent injury of M2 leads to reemergence of hand motor deficits. Considering the importance of the CSP in humans and the common occurrence of lateral frontal cortex injury, these findings suggest that spared supplementary motor cortex may serve as an important therapeutic target that should be considered when designing acute and long-term postinjury patient intervention strategies aimed to enhance the motor recovery process following lateral cortical trauma.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arm / innervation
  • Arm / physiopathology
  • Axons / physiology
  • Axons / ultrastructure
  • Brain Injuries / physiopathology*
  • Brain Mapping
  • Dextrans
  • Disease Models, Animal
  • Female
  • Fluorescein
  • Frontal Lobe / anatomy & histology
  • Frontal Lobe / physiology*
  • Functional Laterality / physiology
  • Interneurons / cytology
  • Interneurons / physiology
  • Macaca mulatta
  • Male
  • Motor Cortex / anatomy & histology
  • Motor Cortex / injuries
  • Motor Cortex / physiology*
  • Motor Neurons / cytology
  • Motor Neurons / physiology
  • Muscle, Skeletal / innervation
  • Muscle, Skeletal / physiopathology
  • Nerve Regeneration / physiology
  • Neuroanatomical Tract-Tracing Techniques
  • Neuronal Plasticity / physiology*
  • Paresis / physiopathology
  • Pyramidal Tracts / anatomy & histology
  • Pyramidal Tracts / physiology*
  • Recovery of Function / physiology
  • Spinal Cord / cytology
  • Spinal Cord / physiology
  • Time
  • Time Factors

Substances

  • Dextrans
  • Fluorescein