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Scientific Understanding of Consciousness |
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Sequential Processing within Broca’s Area
Science 16 October 2009: Vol. 326. no. 5951, pp. 445 - 449 Sequential Processing of Lexical, Grammatical, and Phonological Information Within Broca’s Area Ned T. Sahin,1,2 Steven Pinker,2 Sydney S. Cash,3 Donald Schomer,4 Eric Halgren1 1 Department of Radiology, University of California–San Diego, La Jolla, CA 92037, USA. 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 (~200 milliseconds), grammatical (~320 milliseconds), and phonological (~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. Within cognitive neuroscience, language is understood far less well than sensation, memory, or motor control, because language has no animal homologs, and methods appropriate to humans [functional magnetic resonance imaging (fMRI), studies of brain-damaged patients, and scalp-recorded potentials] are far coarser in space or time than the underlying causal events in neural circuitry. The most comprehensive model of speech production implements linguistic operations as discrete ordered stages, eschewing feedback, loops, parallelism, or cascades. The model posit stages for lexical retrieval (associated with the left middle temporal gyrus at 150 to 225 ms after stimulus presentation), grammatical encoding (locus and duration unknown), phonological retrieval (posterior temporal lobe, 200 to 400 ms), phonological and phonetic processing (Broca’s area, 400 to 600 ms), self-monitoring (superior temporal lobe, beginning at 275 to 400 ms but highly variable in duration), and articulation (motor cortex). Although Broca’s area itself has been identified as the seat of phonology, grammar, and even specific grammatical operations, lesion and neuroimaging studies have tied it to a broad variety of linguistic and nonlinguistic processes. It is possible that grammatical and other linguistic processes are processed distinctly, even sequentially, in the microcircuitry of the brain, but techniques that sum over seconds and centimeters necessarily blur them. In a rare procedure, electrodes are implanted in the brains of patients with epilepsy for clinical evaluation. Recordings of intracranial electrophysiology (ICE) from unaffected brain tissue during periods of normal activity can provide millisecond resolution in time with millimeter resolution in space. Electrodes were located in and around Broca’s area while patients read words verbatim or converted them to an inflected form (past/present or singular/plural).The task engages inflectional morphology, which is like syntax in combining meaningful elements according to grammatical rules, but the units are shorter and semantically simpler, making fewer demands on working memory and conceptual integration, and thus allowing greater experimental control. We applied the high resolution of ICE to a task that distinguishes three linguistic processes to investigate the spatiotemporal patterning of word production in the brain. Of the 26 channels within Broca’s area, the majority (20 of 26) yielded a strong triphasic (three-component) local field potentials (LFP) waveform (9 in patient A, 8 in B, 3 in C). The mean peaks occurred ~200, ~320, and ~450 ms after the target word onset, and this timing was consistent across patients. The three LFP components showed signatures of distinct linguistic processing stages. The ~200-ms component appears to reflect lexical identification. The subsequent two LFP components showed activity patterns predicted for grammatical and phonological processing, respectively. The ~450-ms component reflects phonological, phonetic, and articulatory programming, independently confirmed by its sensitivity to the number of syllables. The triphasic pattern in all patients was found exclusively in Broca’s area. Outside Broca’s area, other patterns prevailed; for example, temporal lobe sites showed a slow and late monophasic component at 500 to 600 ms, possibly reflecting self-monitoring. Although nouns and verbs differ linguistically and neurobiologically, the neuronal activity they evoked was similar. Furthermore, the patterning across inflectional conditions was the same for nouns and verbs. These parallels suggest that words from different lexical classes feed a common process for inflection. Although the language processing stream as a whole surely exhibits parallelism, feedback, and interactivity, the current results support parsimony-based models in which one portion of the stream consists of spatiotemporally distinct processes corresponding to levels of linguistic computation. Among the processes identified by these higher-resolution data is grammatical computation, which has been elusive in previous, coarser-grained investigations. As such, the results are also consistent with recent proposals that Broca’s area is not dedicated to a single kind of linguistic representation but is differentiated into adjacent but distinct circuits that process phonological, grammatical, and lexical information.
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