Perceptual systems controlling speech production

Abstract

It is proposed that the acquisition and maintenance of fluent speech depend on the rapid temporal integration of motor feedforward and polysensory (auditory and somatosensory) feedback signals. In a functional magnetic resonance imaging study on 21 healthy right-handed, English-speaking volunteers, we investigated activity within these motor and sensory pathways and their integration during speech. Four motor conditions were studied: two speech conditions (propositional and nonpropositional speech) and two silent conditions requiring repetitive movement of the principal articulators (jaw and tongue movements). The scanning technique was adapted to minimize artifact associated with overt speech production. Our result indicates that this multimodal convergence occurs within the left and right supratemporal planes (STPs), with peaks of activity at their posteromedial extents, in regions classically considered as unimodal auditory association cortex. This cortical specialization contrasted sharply with the response of somatosensory association cortex (SII), in which activity was suppressed during speech but not during the silent repetitive movement of the principal articulators. It was also clearly distinct from the response of lateral auditory association cortex, which responded to auditory feedback alone, and from that within a left lateralized ventrolateral temporal and inferior frontal system, which served lexical- and sentence-level language retrieval. This response of cortical regions related to speech production is not predicted by the classical model of hierarchical cortical processing, providing new insights into the role of the STP in polysensory integration and into the modulation of activity in SII during normal speech production. These findings have novel implications for the acquisition and maintenance of fluent speech.

Figure 1.

Statistical parametric maps. Sagittal (top), coronal (middle), and axial (bottom) views of the following analyses. Precise localization of all activated areas is detailed in supplemental Table 1 (available at www.jneurosci.org as supplemental material). A, A conjunction of activity of the speech, count, tongue, and jaw conditions, each contrasted with the rest condition. There is a distributed network of bilateral motor activity, involving the medial premotor cortex, the SMA (1), the lateral premotor and primary sensorimotor cortex (2), and cerebellum (3). In addition, there was common activity along the STP and involving the medial and lateral aspects of the planum temporale, particularly evident on the axial view (4). B, A conjunction of activity of speech and count contrasted separately with jaw and tongue. There is bilateral activity within lateral STG (5) lying in the region of auditory parabelt and within motor cortex (6). C, The somatotopy of tongue movement (FDR, p < 0.05): a contrast of tongue against jaw, demonstrating bilateral peaks (7) within primary motor cortex.

Figure 2.

Three networks controlling speech production. A, Color-coded overlays of three separate analyses placed on sagittal T₁-weighted brain slices taken from a single subject template. Distance from the midline is indicated in millimeters. Top row, Left; bottom row, right. B, Plots of mean effect size, with 95% confidence intervals, from specific regions of peak activity. In red is the conjunction of activity during the jaw, tongue, speech, and count conditions, each individually contrasted with the rest condition. In both cerebral hemispheres, common activity distributed along primary sensorimotor cortex within the central sulcus is contiguous with activity along the STP. B1 shows the mean effect size at the peak of activity within the left and right medial planum temporale. In blue is the conjunction of activity in the speech and count conditions contrasted separately with the jaw and tongue conditions. B2 shows the dissociation of activity between the overt speech conditions and the silent conditions involving movements of the jaw and tongue. In yellow is the contrast of the speech and count conditions, demonstrating lateral neocortical activity during propositional speech production. Activity was widely distributed along the length of the left STS, extending ventrally in the posterior left temporal lobe. Although there was bilateral activity, at the statistical threshold used there was evident asymmetry, left ≫ right. Activity was also extensively distributed throughout the left inferior frontal gyrus, including all of Broca's area. On the right, there was a small focus of activity in the caudal right lateral orbitofrontal cortex. B3 shows the left lateralized response of the anterior inferior frontal gyrus to propositional speech. IFG, Inferior frontal gyrus.

Figure 3.

Activity relating to jaw and tongue movements. A, Color overlay of the conjunction of activity in the jaw and tongue conditions, each contrasted separately with the (speech + count) conditions. The overlay is placed on sagittal and coronal T₁-weighted brain slices taken from a single subject template. There was symmetrical activation in three areas: 1, lateral premotor cortex; 2, the Rolandic operculum at the most ventral extreme of the central sulcus, extending into the dorsal insular cortex; and 3, SII within the parietal operculum. B, The plots show mean activity across conditions at peak voxels in left (−64, −28, 30) and right (58, −18, 28) SII, with 95% confidence intervals, for all four conditions relative to the rest condition. There was significant activity during both the jaw and tongue conditions. Activity during the count condition was no different from that during the rest condition, whereas during the speech condition activity was significantly less (suppressed).