Spatiotemporal imaging of cortical activation during verbgeneration and picture namingErik Edwardsa,b,*, Srikantan S. Nagarajanc, Sarang S. Dalalc, Ryan T. Canoltya, Heidi E.Kirschc,d, Nicholas M. Barbaroe, and Robert T. Knightaa Department of Psychology and Helen Wills Neuroscience Institute, University of California,Berkeley, CA, USAb Computer Science & Engineering, University of Washington, Seattle, WA, USAc Department of Radiology, University of California, San Francisco, CA, USAd Department of Neurology, University of California, San Francisco, CA, USAe Department of Neurological Surgery, University of California, San Francisco, CA, USAAbstractOne hundred and fifty years of neurolinguistic research has identified the key structures in the humanbrain that support language. However, neither the classic neuropsychological approaches introducedby Broca (1861) and Wernicke (1874), nor modern neuroimaging employing PET and fMRI hasbeen able to delineate the temporal flow of language processing in the human brain. We recordedthe electrocorticogram (ECoG) from indwelling electrodes over left hemisphere language corticesduring two common language tasks, verb generation and picture naming. We observed that the veryhigh frequencies of the ECoG (high-gamma, 70–160 Hz) track language processing with spatial andtemporal precision. Serial progression of activations is seen at a larger timescale, showing distinctstages of perception, semantic association/selection, and speech production. Within the areassupporting each of these larger processing stages, parallel (or “incremental”) processing is observed.In addition to the traditional posterior vs. anterior localization for speech perception vs. production,we provide novel evidence for the role of premotor cortex in speech perception and of Wernicke’sand surrounding cortex in speech production. The data are discussed with regards to current leadingmodels of speech perception and production, and a “dual ventral stream” hybrid of leading speechperception models is given.KeywordsElectrocorticography; High-gamma; Epilepsy; Speech; LanguageIntroductionHuman language can be studied only indirectly in animal models, and therefore linguisticneuroscience depends critically on methods of human neuroimaging. Human intracranialstudies, using indwelling electrodes in neurosurgical patients, provide a rare opportunity to*Corresponding author. University of Washington, 566 Allen Center, Box 352350, Seattle, WA 98195-2350, USA. Fax: +1 206 6851732. [email protected] (E. Edwards).Competing interests statementThe authors declare no competing financial or other interests.NIH Public AccessAuthor ManuscriptNeuroimage. Author manuscript; available in PMC 2011 March 1.Published in final edited form as:Neuroimage. 2010 March ; 50(1): 291–301. doi:10.1016/j.neuroimage.2009.12.035.NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscriptachieve both high spatial and temporal resolution. Recent ECoG studies in awake patients haveshown that the high-gamma band (γhigh, ~60–300 Hz, typically studied from ~70–160 Hz)provides a powerful means of cortical mapping and detection of task-specific activations(Crone et al., 1998, 2001; Edwards et al., 2005; Canolty et al., 2007; Towle et al., 2008; Edwardset al., 2009). Furthermore, γhigh has emerged as the strongest electrophysiological correlate ofcortical blood-flow (Logothetis et al., 2001; Brovelli et al., 2005; Mukamel et al., 2005;Niessing et al., 2005; Lachaux et al., 2007), often showing even higher correlations with blood-flow measures than multi-unit spiking activity. The γhigh band also exhibits excellent signal-to-noise ratio (SNR), with event-related increases clearly seen at the single-trial level or afteraveraging only a few trials (see Figs. 2d–5d below). The present study uses these advantagesof the γhigh band to study the topography and temporal sequence of cortical activations duringtwo common language tasks, verb generation and picture naming.Verb generation (Petersen et al., 1988, 1989) is a semantic association task where a noun ispresented and the subject responds with an associated verb. Recent neurosurgical studiesemphasize the verb generation task for use in preoperative and intraoperative languagemapping (Herholz et al., 1997; Thiel et al., 1998; Ojemann et al., 2002). Picture naming is acommon language task employed in neurosurgical language mapping (Penfield and Roberts,1959; Ojemann et al., 1989; Sinai et al., 2005) and aphasia assessment (Goodglass et al.,2000). This task has similar speech production requirements as verb generation (speaking asingle word), but may not activate semantic areas as strongly (Herholz et al., 1997). For picturenaming, there is usually only one correct answer, and the task of associating a concretelypresented object with a noun is one of the earliest linguistic skills mastered developmentally.In verb generation, the patient must creatively link a noun to a verb with freedom to chooseamongst competing response alternatives, requiring more executive-level semantic selection(Thompson-Schill et al., 1998). The available evidence consistently implicates inferior andmiddle frontal gyri (IFG and MFG), in addition to other widely distributed cortical areas, inthe semantic association/selection aspects of the verb generation task (Petersen et al., 1988;Herholz et al., 1997; Thiel et al., 1998; Thompson-Schill et al., 1998; Ojemann et al., 2002).The ECoG method does not allow complete or arbitrary spatial coverage, since the electrodeplacements are determined for clinical purposes, so we will not be able to study the full networkinvolved in “semantics”, and will limit our scope to the areas that do find exposure in ourcohort.In the version of the verb generation task used here, the stimulus is an auditorily presentednoun, allowing the study of single-word speech processing. In the Supplementary Information(SI), we also present results for other auditory and speech processing tasks performed in thesame patients. Receptive speech has traditionally been associated with Wernicke’s (1874) areaof the posterior superior temporal gyrus (STG) and surrounding areas. Current models ofspeech perception include greater Wernicke’s area, but also implicate a “dorsal” stream thatincludes regions also involved in speech motor processing (Hickok and Poeppel, 2007). Theinvolvement of motor areas in speech perception was foreshadowed in a