The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients

Abstract

Although the role of the premotor cortex (PMC) was widely studied in motor function, very few data are currently available about the participation of this structure in language. We report a series of 25 right-handed patients harboring a low-grade glioma near or within the left dominant PMC, operated on under local anesthesia with intraoperative real-time sensorimotor and language mappings using electrical stimulations all along the resection. Language tasks consisted of counting and picture naming (preceded by the reading of a short sentence). Stimulations of the left PMC induced transient speech disturbances in all patients, with disruption of both counting and reading/naming during stimulation of the ventral PMC—due to elicitation of an anarthria—while generating an anomia during stimulation of the dorsal PMC. Moreover, corresponding subcortical pathways generated the same language disorders as at the cortical level when stimulated. Eloquent structures were systematically preserved, allowing the avoidance of definitive postoperative deficit. These findings suggest first that the left dominant PMC seems to play a major role in language and second that this structure could have a well-ordered functional organization, namely with the ventral PMC, which might be involved in planification of articulation, and the dorsal PMC, which might be involved in the naming network.

Introduction

The human premotor cortex (PMC) was delineated by Fulton (Fulton, 1935) as the frontal agranular cortex (area 6) rostral to the primary motor cortex (area 4). This structure was divided into two subregions (Freund, 1996):

• the ventral PMC, i.e., the ventral compartment of area 6 (area 6aα) (Vogt and Vogt, 1919) covering the anterior part of the precentral gyrus;

• the dorsal PMC, i.e., the dorsal part of area 6 (area 6aβ) (Vogt and Vogt, 1919), covering the posterior part of the superior and middle frontal gyri, in front of the precentral sulcus.

Although many lesion Freund and Hummelsheim 1985, Halsband and Freund 1990, stimulation Foerster 1936, Lüders et al 1995, and functional neuroimaging Colebatch et al 1991, Deiber et al 1991, Seitz and Roland 1992 human studies allowed better clarification of the implication of the PMC in motor function, the participation of this area in language remains poorly understood. Some authors nevertheless advocated the involvement of dominant PMC in writing and reading Dehaene et al 2001, Exner 1881, Ritaccio et al 1992 and in speech production Alexander et al 1989, Cohen et al 1993, Fox et al 2001, Luria 1966. Moreover, recent works using positron emission tomography (PET) or fMRI found PMC activation during naming Chao and Martin 2000, Grabowski et al 1998, Grafton et al 1997, Martin et al 1996 and speech (Wise et al., 1999).

The present work reports a series of 25 patients harboring a cerebral low-grade glioma near or within the left dominant PMC, operated on under local anesthesia with intraoperative sensorimotor and language mappings using electrical stimulations. On the basis of the functional findings collected during surgery, the role of the left PMC in language is discussed and the therapeutic implications are considered.