Limited plastic potential of the left ventral premotor cortex in speech articulation: evidence from intraoperative awake mapping in glioma patients

Hum Brain Mapp. 2014 Apr;35(4):1587-96. doi: 10.1002/hbm.22275. Epub 2013 Apr 24.

Abstract

Objectives: Despite previous lesional and functional neuroimaging studies, the actual role of the left ventral premotor cortex (vPMC), i.e., the lateral part of the precentral gyrus, is still poorly known.

Experimental design: We report a series of eight patients with a glioma involving the left vPMC, who underwent awake surgery with intraoperative cortical and subcortical language mapping. The function of the vPMC, its subcortical connections, and its reorganization potential are investigated in the light of surgical findings and language outcome after resection.

Principal observations: Electrostimulation of both the vPMC and subcortical white matter tract underneath the vPMC, that is, the anterior segment of the lateral part of the superior longitudinal fascicle (SLF), induced speech production disturbances with anarthria in all cases. Moreover, although some degrees of redistribution of the vPMC have been found in four patients, allowing its partial resection with no permanent speech disorders, this area was nonetheless still detected more medially in the precentral gyrus in the eight patients, despite its invasion by the glioma. Moreover, a direct connection of the vPMC with the SLF was preserved in all cases.

Conclusions: Our original data suggest that the vPMC plays a crucial role in the speech production network and that its plastic potential is limited. We propose that this limitation is due to an anatomical constraint, namely the necessity for the left vPMC to remain connected to the lateral SLF. Beyond fundamental implications, such knowledge may have clinical applications, especially in surgery for tumors involving this cortico-subcortical circuit.

Keywords: awake surgery; brain plasticity; speech articulation; subcortical electrostimulation; superior longitudinal fascicle; ventral premotor cortex.

MeSH terms

  • Adult
  • Brain Mapping
  • Brain Neoplasms / pathology
  • Brain Neoplasms / physiopathology*
  • Brain Neoplasms / surgery
  • Electric Stimulation
  • Female
  • Frontal Lobe / pathology
  • Frontal Lobe / physiopathology*
  • Frontal Lobe / surgery
  • Functional Laterality
  • Glioma / pathology
  • Glioma / physiopathology*
  • Glioma / surgery
  • Humans
  • Intraoperative Neurophysiological Monitoring
  • Language
  • Language Tests
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Nerve Fibers, Myelinated / pathology
  • Nerve Fibers, Myelinated / physiology
  • Neural Pathways / pathology
  • Neural Pathways / physiopathology
  • Neural Pathways / surgery
  • Neuronal Plasticity / physiology
  • Speech / physiology*
  • Speech Disorders / pathology
  • Speech Disorders / physiopathology
  • Wakefulness / physiology
  • Young Adult