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Sequential processing of lexical, grammatical, and phonological information within Broca's area - PubMed

  • ️Thu Jan 01 2009

Sequential processing of lexical, grammatical, and phonological information within Broca's area

Ned T Sahin et al. Science. 2009.

Abstract

Words, grammar, and phonology are linguistically distinct, yet their neural substrates are difficult to distinguish in macroscopic brain regions. We investigated whether they can be separated in time and space at the circuit level using intracranial electrophysiology (ICE), namely by recording local field potentials from populations of neurons using electrodes implanted in language-related brain regions while people read words verbatim or grammatically inflected them (present/past or singular/plural). Neighboring probes within Broca's area revealed distinct neuronal activity for lexical (approximately 200 milliseconds), grammatical (approximately 320 milliseconds), and phonological (approximately 450 milliseconds) processing, identically for nouns and verbs, in a region activated in the same patients and task in functional magnetic resonance imaging. This suggests that a linguistic processing sequence predicted on computational grounds is implemented in the brain in fine-grained spatiotemporally patterned activity.

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Figures

Fig. 1
Fig. 1

Experimental design. (A) Structure of trials. (B) Experimental conditions, example trials, and required psycholinguistic processes. (C) Hypothesized patterns of neural activity by condition, for inflectional and phonological processing.

Fig. 2
Fig. 2

Main Results: sequential processing of lexical, grammatical, and phonological information in overlapping circuits. (A) (Top) Neural activity recorded from several channels within Broca’s area (Patient A, Brodmann area 45) shows three LFP components that were consistently evoked by the task (~200, ~320, ~450 ms). (Bottom) The ~200 ms component is sensitive to word frequency but not word length, suggesting that it indexes a cognitive process (for instance, lexical identification), not simply perception. Stacked waveforms (top and bottom) conform to the axes noted on the first waveform. (B) At ~320 ms, the LFP pattern suggests inflectional processing. (C) At ~450 ms, in a channel 5mm distant, the complementary pattern suggests phonological processing. (Inset) MRI slices from this patient, annotated with the anatomical location of A4, the electrode contact in common to the two recording channels reported in (B) and (C). (General): Statistical significance: **** (P < 0.0001), *** (P < 0.001), ** (P < 0.01) (t-test: one tail, two-sample, equal variance). Box arrows (bottom row) indicate linguistic processing stages; these may be interposed among other stages not addressed by the present study.

Fig. 3
Fig. 3

Localization of fMRI responses, depth electrodes, and neural generators. (A) fMRI in 18 controls, contrasting activity for all task conditions with visual-fixation baseline periods. The task engages classic language areas (Broca’s, speech-related motor cortex, medial supplementary motor area, anterior cingulate, superior temporal lobe), and visual-reading areas (visual wordform area, primary and ventral visual cortex). Classic Broca’s area is circled. Thresholding and correction at a 0.01 false discovery rate (16) – scale as in (B). (B, C) Single-patient fMRI (identical contrast) reveals similar activations in both patients and controls. Surfaces are inflated to reveal activation within sulci. (D) Co-registered MRI and computerized tomography (CT) scan of Patient C showing depth probes inserted through the skull. (E) Intra-operative photo showing left perisylvian language areas. Letters: insertion points of the probes; dashed lines: surface projections of their intracortical trajectories. Putative Brodmann areas are labeled. (F) Post-implantation MRI reveals that Probe B traverses Broca’s area in the postero-medial process of IFG par opercularis facing the insula; and pre-implantation fMRI (G) demonstrates that the region was activated by the task in this patient. (H) Location of Probe A, in Broca’s area traversing IFG pars triangularis within the inferior frontal sulcus. (I, J) Schematic of neural dipoles near Probe A that generated the LFP components, hypothesized from their polarities, amplitudes and locations (see fig. S3). Schematic gyral outline corresponds to the gyral trace superimposed on the MRI in (H).

Fig. 4
Fig. 4

Additional features of the triphasic waveform support the lexical-inflectional-phonological progression. (A) Triphasic activity is specific to Broca’s area, and consistent across patients. All-condition average waveforms from task-active channels in each patient are superimposed (scaled in amplitude to a single channel in each region and standardized in polarity). (B) Noun (black) and verb (red) inflection (Null and Overt combined) involved nearly identical neural activity, across sites and patients. Standardized across channels in polarity. (C) The ~450 ms component, which is sensitive to phonological differences among inflectional conditions, is also sensitive to phonological complexity (syllable count) of the target word (p<0.01, corrected). (D) Neural activity in Broca’s area is evoked primarily when processing the target word (when the linguistic processing of interest should occur), not the cue (35).

Comment in

  • Neuroscience. The speaking brain.

    Hagoort P, Levelt WJ. Hagoort P, et al. Science. 2009 Oct 16;326(5951):372-3. doi: 10.1126/science.1181675. Science. 2009. PMID: 19833945 No abstract available.

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