Elsevier

NeuroImage

Volume 50, Issue 1, March 2010, Pages 291-301
NeuroImage

Spatiotemporal imaging of cortical activation during verb generation and picture naming

https://doi.org/10.1016/j.neuroimage.2009.12.035Get rights and content

Abstract

One hundred and fifty years of neurolinguistic research has identified the key structures in the human brain that support language. However, neither the classic neuropsychological approaches introduced by Broca, 1861, Wernicke, 1874, nor modern neuroimaging employing PET and fMRI has been able to delineate the temporal flow of language processing in the human brain. We recorded the electrocorticogram (ECoG) from indwelling electrodes over left hemisphere language cortices during two common language tasks, verb generation and picture naming. We observed that the very high frequencies of the ECoG (high-gamma, 70–160 Hz) track language processing with spatial and temporal precision. Serial progression of activations is seen at a larger timescale, showing distinct stages of perception, semantic association/selection, and speech production. Within the areas supporting 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's and surrounding cortex in speech production. The data are discussed with regards to current leading models of speech perception and production, and a “dual ventral stream” hybrid of leading speech perception models is given.

Introduction

Human language can be studied only indirectly in animal models, and therefore linguistic neuroscience depends critically on methods of human neuroimaging. Human intracranial studies, using indwelling electrodes in neurosurgical patients, provide a rare opportunity to achieve both high spatial and temporal resolution. Recent ECoG studies in awake patients have shown 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, Crone et al., 2001, Edwards et al., 2005, Canolty et al., 2007, Towle et al., 2008, Edwards et al., 2009). Furthermore, γhigh has emerged as the strongest electrophysiological correlate of cortical 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 after averaging only a few trials (see Fig. 2, Fig. 3, Fig. 4, Fig. 5 below). The present study uses these advantages of the γhigh band to study the topography and temporal sequence of cortical activations during two common language tasks, verb generation and picture naming.

Verb generation (Petersen et al., 1988, Petersen et al., 1989) is a semantic association task where a noun is presented and the subject responds with an associated verb. Recent neurosurgical studies emphasize the verb generation task for use in preoperative and intraoperative language mapping (Herholz et al., 1997, Thiel et al., 1998, Ojemann et al., 2002). Picture naming is a common 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 a single word), but may not activate semantic areas as strongly (Herholz et al., 1997). For picture naming, there is usually only one correct answer, and the task of associating a concretely presented 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 choose amongst competing response alternatives, requiring more executive-level semantic selection (Thompson-Schill et al., 1998). The available evidence consistently implicates inferior and middle frontal gyri (IFG and MFG), in addition to other widely distributed cortical areas, in the 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 electrode placements are determined for clinical purposes, so we will not be able to study the full network involved in “semantics”, and will limit our scope to the areas that do find exposure in our cohort.

In the version of the verb generation task used here, the stimulus is an auditorily presented noun, 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 the same patients. Receptive speech has traditionally been associated with Wernicke's (1874) area of the posterior superior temporal gyrus (STG) and surrounding areas. Current models of speech perception include greater Wernicke's area, but also implicate a “dorsal” stream that includes regions also involved in speech motor processing (Hickok and Poeppel, 2007). The involvement of motor areas in speech perception was foreshadowed in a long tradition of motor theories of speech perception (Liberman et al., 1967), but neuroimaging evidence was only recently obtained (Wilson et al., 2004, Meister et al., 2007).

Verb generation and picture naming involve similar speech production requirements, allowing within-subject confirmation of single-word speech production activations with two distinct “lead-in” tasks. One of the outstanding questions for speech production is the possible role of posterior (Wernicke's and surrounding) areas traditionally associated with speech perception. There is now strong evidence for a motor speech area of the posterior superior temporal plane (STP) near to or overlapping with the temporal–parietal junction (TPJ), a finding foreshadowed in earlier studies of conduction aphasia (Wise et al., 2001, Bates et al., 2003, Buchsbaum et al., 2005, Hickok and Poeppel, 2007). Another outstanding question in speech production is which cortical regions are involved in preparing the phonological representation used to guide articulation. A leading model (Levelt, 1999, Indefrey and Levelt, 2004) implicates the posterior STG (pSTG), but we present here the first evidence combining high spatial and temporal resolution and arrive at a different conclusion.

Section snippets

Patients

A total of 4 patients (3 ♀, 1 ♂) with intractable epilepsy were studied several days after surgery for implantation of subdural electrodes. All patients were right-handed, native English speakers, and all were left-hemisphere dominant as assessed by a pre-operative intracarotid amobarbital test using picture naming (full details in Loring et al., 1997). The age range was 15–45 y.o. (Patient 1: 39 y.o. ♀; Patient 2: 37 y.o. ♀; Patient 3: 15 y.o. ♂; Patient 4: 45 y.o. ♀). The seizures had begun

Results

Auditory, motor, and language tasks were performed over the course of 2–3 days in each patient, including the verb generation and picture naming tasks. The SI gives complementary results from additional auditory tasks. TF analysis of the ECoG used a Gaussian filter-bank and the Hilbert transform, yielding a time-series of analytic amplitude (AA, envelope of the filtered signal) for each frequency band. We focus on γhigh (averaged over the range 70–160 Hz), since this band shows the most robust

Discussion

We have used the unique advantages of ECoG γhigh mapping (Crone et al., 2006) to study cortical language processing during verb generation and picture naming. Taken together, the results show consistent agreement of γhigh activation topographies with results of functional imaging studies, adding further evidence to the strong empirical relation of γhigh levels to measures of blood-flow (Darrow and Graf, 1945, Logothetis et al., 2001, Brovelli et al., 2005, Mukamel et al., 2005, Niessing et al.,

Competing interests statement

The authors declare no competing financial or other interests.

Acknowledgments

We thank Eddie F. Chang, Clay C. Clayworth, Leon Y. Deouell, Noa Fogelson, and Maryam Soltani for input and assistance.

This work was supported by NINDS grant NS21135, NIH grants DC006435 and DC4855, and NINDS fellowship F32-NS061616.

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