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From phonemes to articulatory codes: an fMRI study of the role of Broca's area in speech production.

ABSTRACT: We used event-related functional magnetic resonance imaging to investigate the neuroanatomical substrates of phonetic encoding and the generation of articulatory codes from phonological representations. Our focus was on the role of the left inferior frontal gyrus (LIFG) and in particular whether the LIFG plays a role in sublexical phonological processing such as syllabification or whether it is directly involved in phonetic encoding and the generation of articulatory codes. To answer this question, we contrasted the brain activation patterns elicited by pseudowords with high- or low-sublexical frequency components, which we expected would reveal areas related to the generation of articulatory codes but not areas related to phonological encoding. We found significant activation of a premotor network consisting of the dorsal precentral gyrus, the inferior frontal gyrus bilaterally, and the supplementary motor area for low- versus high-sublexical frequency pseudowords. Based on our hypothesis, we concluded that these areas and in particular the LIFG are involved in phonetic and not phonological encoding. We further discuss our findings with respect to the mechanisms of phonetic encoding and provide evidence in support of a functional segregation of the posterior part of Broca's area, the pars opercularis.

SUBMITTER: Papoutsi M

PROVIDER: S-EPMC2722428 | biostudies-literature | 2009 Sep

REPOSITORIES: biostudies-literature

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From phonemes to articulatory codes: an fMRI study of the role of Broca's area in speech production.

Papoutsi Marina M de Zwart Jacco A JA Jansma J Martijn JM Pickering Martin J MJ Bednar James A JA Horwitz Barry B

Cerebral cortex (New York, N.Y. : 1991) 20090129 9

We used event-related functional magnetic resonance imaging to investigate the neuroanatomical substrates of phonetic encoding and the generation of articulatory codes from phonological representations. Our focus was on the role of the left inferior frontal gyrus (LIFG) and in particular whether the LIFG plays a role in sublexical phonological processing such as syllabification or whether it is directly involved in phonetic encoding and the generation of articulatory codes. To answer this questi ...[more]

PMID: 19181696

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Project description:BackgroundThe association between brain regions involved in speech production and those that play a role in speech perception is not yet fully understood. We compared speech production related brain activity with activations resulting from perceptual categorization of syllables using high field 7 Tesla functional magnetic resonance imaging (fMRI) at 1-mm isotropic voxel resolution, enabling high localization accuracy compared to previous studies.MethodsBlood oxygenation level dependent (BOLD) signals were obtained in 20 normal hearing subjects using a simultaneous multi-slice (SMS) 7T echo-planar imaging (EPI) acquisition with whole-head coverage and 1 mm isotropic resolution. In a speech production localizer task, subjects were asked to produce a silent lip-round vowel /u/ in response to the visual cue "U" or purse their lips when they saw the cue "P". In a phoneme discrimination task, subjects were presented with pairs of syllables, which were equiprobably identical or different along an 8-step continuum between the prototypic /ba/ and /da/ sounds. After the presentation of each stimulus pair, the subjects were asked to indicate whether the two syllables they heard were identical or different by pressing one of two buttons. In a phoneme classification task, the subjects heard only one syllable and asked to indicate whether it was /ba/ or /da/.ResultsUnivariate fMRI analyses using a parametric modulation approach suggested that left motor, premotor, and frontal cortex BOLD activations correlate with phoneme category variability in the /ba/-/da/ discrimination task. In contrast, the variability related to acoustic features of the phonemes were the highest in the right primary auditory cortex. Our multivariate pattern analysis (MVPA) suggested that left precentral/inferior frontal cortex areas, which were associated with speech production according to the localizer task, play a role also in perceptual categorization of the syllables.ConclusionsThe results support the hypothesis that articulatory motor networks in the left hemisphere that are activated during speech production could also have a role in perceptual categorization of syllables. Importantly, high voxel-resolution combined with advanced coil technology allowed us to pinpoint the exact brain regions involved in both perception and production tasks.

Project description:The exact nature of the role of Broca's area in control of speech and whether it is exerted at the cognitive or at the motor level is still debated. Intraoperative evidence of a lack of motor responses to direct electrical stimulation (DES) of Broca's area and the observation that its stimulation induces a "speech arrest" without an apparent effect on the ongoing activity of phono-articulatory muscles, raises the argument. Essentially, attribution of direct involvement of Broca's area in motor control of speech, requires evidence of a functional connection of this area with the phono-articulatory muscles' motoneurons. With a quantitative approach we investigated, in 20 patients undergoing surgery for brain tumors, whether DES delivered on Broca's area affects the recruitment of the phono-articulatory muscles' motor units. The electromyography (EMG) of the muscles active during two speech tasks (object picture naming and counting) was recorded during and in absence of DES on Broca's area. Offline, the EMG of each muscle was analyzed in frequency (power spectrum, PS) and time domain (root mean square, RMS) and the two conditions compared. Results show that DES on Broca's area induces an intensity-dependent "speech arrest." The intensity of DES needed to induce "speech arrest" when applied on Broca's area was higher when compared to the intensity effective on the neighboring pre-motor/motor cortices. Notably, PS and RMS measured on the EMG recorded during "speech arrest" were superimposable to those recorded at baseline. Partial interruptions of speech were not observed. Speech arrest was an "all-or-none" effect: muscle activation started only by removing DES, as if DES prevented speech onset. The same effect was observed when stimulating directly the subcortical fibers running below Broca's area. Intraoperative data point to Broca's area as a functional gate authorizing the phonetic translation to be executed by the motor areas. Given the absence of a direct effect on motor units recruitment, a direct control of Broca's area on the phono-articulatory apparatus seems unlikely. Moreover, the strict correlation between DES-intensity and speech prevention, might attribute this effect to the inactivation of the subcortical fibers rather than to Broca's cortical neurons.

Project description:Broca's area in the posterior half of the left inferior frontal gyrus has long been thought to be critical for speech production. The current view is that long-term speech production outcome in patients with Broca's area damage is best explained by the combination of damage to Broca's area and neighbouring regions including the underlying white matter, which was also damaged in Paul Broca's two historic cases. Here, we dissociate the effect of damage to Broca's area from the effect of damage to surrounding areas by studying long-term speech production outcome in 134 stroke survivors with relatively circumscribed left frontal lobe lesions that spared posterior speech production areas in lateral inferior parietal and superior temporal association cortices. Collectively, these patients had varying degrees of damage to one or more of nine atlas-based grey or white matter regions: Brodmann areas 44 and 45 (together known as Broca's area), ventral premotor cortex, primary motor cortex, insula, putamen, the anterior segment of the arcuate fasciculus, uncinate fasciculus and frontal aslant tract. Spoken picture description scores from the Comprehensive Aphasia Test were used as the outcome measure. Multiple regression analyses allowed us to tease apart the contribution of other variables influencing speech production abilities such as total lesion volume and time post-stroke. We found that, in our sample of patients with left frontal damage, long-term speech production impairments (lasting beyond 3 months post-stroke) were solely predicted by the degree of damage to white matter, directly above the insula, in the vicinity of the anterior part of the arcuate fasciculus, with no contribution from the degree of damage to Broca's area (as confirmed with Bayesian statistics). The effect of white matter damage cannot be explained by a disconnection of Broca's area, because speech production scores were worse after damage to the anterior arcuate fasciculus with relative sparing of Broca's area than after damage to Broca's area with relative sparing of the anterior arcuate fasciculus. Our findings provide evidence for three novel conclusions: (i) Broca's area damage does not contribute to long-term speech production outcome after left frontal lobe strokes; (ii) persistent speech production impairments after damage to the anterior arcuate fasciculus cannot be explained by a disconnection of Broca's area; and (iii) the prior association between persistent speech production impairments and Broca's area damage can be explained by co-occurring white matter damage, above the insula, in the vicinity of the anterior part of the arcuate fasciculus.

Dataset Information

From phonemes to articulatory codes: an fMRI study of the role of Broca's area in speech production.

Publications

From phonemes to articulatory codes: an fMRI study of the role of Broca's area in speech production.

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