Sensory–motor transformations for speech occur bilaterally

Abstract

Historically, the study of speech processing has emphasized a strong link between auditory perceptual input and motor production output1–4. A kind of ‘parity’ is essential, as both perception- and production-based representations must form a unified interface to facilitate access to higher order language processes such as syntax and semantics, believed to be computed in the dominant, typically left hemisphere5,6. While various theories have been proposed to unite perception and production2,7, the underlying neural mechanisms are unclear. Early models of speech and language processing proposed that perceptual processing occurred in the left posterior superior temporal gyrus (Wernicke’s area) and motor production processes occurred in the left inferior frontal gyrus (Broca’s area)8,9. Sensory activity was proposed to link to production activity via connecting fiber tracts, forming the left lateralized speech sensory-motor system10. While recent evidence indicates that speech perception occurs bilaterally11–13, prevailing models maintain that the speech sensory-motor system is left lateralized11,14–18 and facilitates the transformation from sensory-based auditory representations to motor-based production representations11,15,16. Evidence for the lateralized computation of sensory-motor speech transformations is, however, indirect and primarily comes from lesion patients with speech repetition deficits (conduction aphasia) and studies using covert speech and hemodynamic functional imaging16,19. Whether the speech sensory-motor system is lateralized like higher order language processes, or bilateral, like speech perception is controversial. Here, using direct neural recordings in subjects performing sensory-motor tasks involving overt speech production, we show that sensory-motor transformations occur bilaterally. We demonstrate that electrodes over bilateral inferior frontal, inferior parietal, superior temporal, premotor, and somatosensory cortices exhibit robust sensory-motor neural responses during both perception and production in an overt word repetition task. Using a non-word transformation task, we show that bilateral sensory-motor responses can perform transformations between speech perception- and production-based representations. These results establish a bilateral sublexical speech sensory-motor system.

Bilateral dorsal and ventral fiber pathways for the processing of affective prosody identified by probabilistic fiber tracking

“…However, since we have not directly compared this anatomical prosody network with other specific networks, especially the semantic language processing network, we cannot rule out the possibility that some of the connections also underlie other speech-related, or even general auditory functions. For example, some aspects of speech processing also involve the right hemisphere (Cogan et al, 2014;Hickok and Poeppel, 2007). Further studies are thus needed to determine if the anatomical connections described here are specific for affective prosody processing only, or if they are shared for the processing of other auditory stimuli.…”

Redefining the role of Broca’s area in speech

“…Pseudowords were created by substituting one phoneme from a matched list of real words. Real words and pseudowords were matched for the following sublexical properties: phonological neighborhood density (range [15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30], biphoneme probability (range 0.0001-0.0039), and positional probability (range 0.011-0.065). Estimates are in log units, calculated using the Irvine Phonotactic Online Dictionary (31).…”

“…In contrast, direct intracranial cortical recordings offer a unique opportunity to acquire neural signals with an unprecedented combination of temporal and spatial resolution. Several such studies have implicated the inferior frontal lobe in word production (14)(15)(16)(17)(18)(19), but did not focus on the specific role of Broca's area in production. Conversely, a recent intracranial study was, to our knowledge, the first to focus on Broca's area, finding evidence for lexical, grammatical, and phonological processing (20), but did not examine the processes required for overt word production (phonetic encoding and articulation).…”

The peri-Sylvian cortical network underlying single word repetition revealed by electrocortical stimulation and direct neural recordings

“…However, there are several interesting case studies indicating that damage to the arcuate fasciculus is not a necessary condition for conduction aphasia (Quigg & Fountain, 1999; Quigg, Geldmacher, & Elias, 2006), and that it may not play a specific role in sensorimotor translation (Dick & Tremblay, 2012). There is also recent evidence that the sensorimotor transformations required for verbal repetition are bilateral (Cogan et al, 2014). Furthermore, recent quantitative morphometric neuroimaging analyses have suggested that damage to cortical gray matter in posterior temporo-parietal regions is more closely associated with the repetition deficits observed in a variety of aphasia disorders (Rogalsky et al, 2015).…”