title: Intraoperative mapping during repeat awake craniotomy reveals the functional plasticity of adult cortex.
abstract: OBJECT To avoid iatrogenic injury during the removal of intrinsic cerebral neoplasms such as gliomas, direct electrical stimulation (DES) is used to identify cortical and subcortical white matter pathways critical for language, motor, and sensory function. When a patient undergoes more than 1 brain tumor resection as in the case of tumor recurrence, the use of DES provides an unusual opportunity to examine brain plasticity in the setting of neurological disease. METHODS The authors examined 561 consecutive cases in which patients underwent DES mapping during surgery forglioma resection. "Positive" and "negative" sites-discrete cortical regions where electrical stimulation did (positive) or did not (negative) produce transient sensory, motor, or language disturbance-were identified prior to tumor resection and documented by intraoperative photography for categorization into functional maps. In this group of 561 patients, 18 were identified who underwent repeat surgery in which 1 or more stimulation sites overlapped with those tested during the initial surgery. The authors compared intraoperative sensory, motor, or language mapping results between initial and repeat surgeries, and evaluated the clinical outcomes for these patients. RESULTS A total of 117 sites were tested for sensory (7 sites, 6.0%), motor (9 sites, 7.7%), or language (101 sites, 86.3%) function during both initial and repeat surgeries. The mean interval between surgical procedures was 4.1 years. During initial surgeries, 95 (81.2%) of 117 sites were found to be negative and 22 (18.8%) of 117 sites were found to be positive. During repeat surgeries, 103 (88.0%) of 117 sites were negative and 14 (12.0%) of 117 were positive. Of the 95 sites that were negative at the initial surgery, 94 (98.9%) were also negative at the repeat surgery, while 1 (1.1%) site was found to be positive. Of the 22 sites that were initially positive, 13 (59.1%) remained positive at repeat surgery, while 9 (40.9%) had become negative for function. Overall, 6 (33.3%) of 18 patients exhibited loss of function at 1 or more motor or language sites between surgeries. Loss of function at these sites was not associated with neurological impairment at the time of repeat surgery, suggesting that neurological function was preserved through neural circuit reorganization or activation of latent functional pathways. CONCLUSIONS The adult central nervous system reorganizes motor and language areas in patients with glioma. Ultimately, adult neural plasticity may help to preserve motor and language function in the presence of evolving structural lesions. The insight gained from this subset of patients has implications for our understanding of brain plasticity in clinical settings.
authors.affiliation: Department of Neurological Surgery, University of California, San Francisco, California.
authors.forename: Derek G
authors.initials: DG
authors.lastname: Southwell
authors.affiliation: Department of Neurological Surgery, University of California, San Francisco, California.
authors.forename: Shawn L
authors.initials: SL
authors.lastname: Hervey-Jumper
authors.affiliation: Department of Neurological Surgery, University of California, San Francisco, California.
authors.forename: David W
authors.initials: DW
authors.lastname: Perry
authors.affiliation: Department of Neurological Surgery, University of California, San Francisco, California.
authors.forename: Mitchel S
authors.initials: MS
authors.lastname: Berger
mesh_terms: D000328:Adult; D001931:Brain Mapping / Q000379:methods*; D001932:Brain Neoplasms / Q000503:physiopathology / Q000601:surgery*; D002540:Cerebral Cortex / Q000503:physiopathology* / Q000601:surgery*; D016292:Procedural Sedation; D003399:Craniotomy / Q000379:methods*; D004558:Electric Stimulation; D005260:Female; D005910:Glioma / Q000503:physiopathology / Q000601:surgery*; D006801:Humans; D007432:Intraoperative Period; D008297:Male; D008875:Middle Aged; D016343:Monitoring, Intraoperative; D009364:Neoplasm Recurrence, Local / Q000503:physiopathology / Q000601:surgery*; D009416:Nerve Regeneration / Q000502:physiology; D009460:Neurologic Examination; D009473:Neuronal Plasticity / Q000502:physiology*; D012086:Reoperation; D012189:Retrospective Studies; D047368:Tumor Burden / Q000502:physiology
keywords: ADP = after-discharge potential; DES = direct electrical stimulation; FLAIR = fluid-attenuated inversion-recovery; GTR = gross-total resection; PET = positron emission tomography; STR = subtotal resection; TMS = transcranial magnetic stimulation; WHO = World Health Organization; awake craniotomy; brain plasticity; direct electrical stimulation; fMRI = functional MRI; glioma; surgical technique