Scientific Understanding of Consciousness
Speech Sensory–Motor Transformations occur Bilaterally
Nature 507, 94–98 (06 March 2014)
Sensory–motor transformations for speech occur bilaterally
Gregory B. Cogan, Thomas Thesen, Chad Carlson, Werner Doyle, Orrin Devinsky & Bijan Pesaran
Center for Neural Science, New York University, New York, New York 10003, USA
Department of Neurology, New York University School of Medicine, New York, New York 10016, USA
Department of Neurosurgery, New York University School of Medicine, New York, New York 10016, USA
Historically, the study of speech processing has emphasized a strong link between auditory perceptual input and motor production output. 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 hemisphere. Although various theories have been proposed to unite perception and production, 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). Sensory activity was proposed to link to production activity through connecting fibre tracts, forming the left lateralized speech sensory–motor system. Although recent evidence indicates that speech perception occurs bilaterally, prevailing models maintain that the speech sensory–motor system is left lateralized and facilitates the transformation from sensory-based auditory representations to motor-based production representations. However, evidence for the lateralized computation of sensory–motor speech transformations is indirect and primarily comes from stroke patients that have speech repetition deficits (conduction aphasia) and studies using covert speech and haemodynamic functional imaging. Whether the speech sensory–motor system is lateralized, like higher-order language processes, or bilateral, like speech perception, is controversial. Here we use direct neural recordings in subjects performing sensory–motor tasks involving overt speech production to 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 speech-production-based representations. These results establish a bilateral sublexical speech sensory–motor system.
To investigate the sensory–motor representations that link speech perception and production, we used electrocorticography (ECoG), in which electrical recordings of neural activity are made directly from the cortical surface in a group of patients with pharmacologically intractable epilepsy. ECoG is an important electrophysiological signal recording modality that combines excellent temporal resolution with good spatial localization. Critically for this study, ECoG data contain limited artefacts due to muscle and movements during speech production compared with non-invasive methods that suffer artefacts with jaw movement. Thus, using ECoG we were able to investigate directly neural representations for sensory–motor transformations using overt speech production.
Sixteen patients with subdural electrodes implanted in the left hemisphere (6 subjects), right hemisphere (7 subjects) or both hemispheres (3 subjects) performed variants of an overt word repetition task designed to elicit sensory–motor activations. We observed increases in neural activity across the high gamma frequency range (60–200 Hz and above) with maximal activity across subjects between 70–90 Hz. High gamma activity reflects the spiking activity of populations of neurons during task performance. Individual electrodes showed one of three types of task responses: sensory–motor (S-M), production (PROD), or auditory (AUD). We found that AUD activity was generally localized to the superior temporal gyrus and middle temporal gyrus (42 out of 57 electrodes (74%); and PROD activity occurred mostly in the motor and premotor corticies, somatosensory cortex, and the inferior parietal lobule (98 out of 124 electrodes (79%); consistent with previous models and results of speech-perception and -production studies. Furthermore, electrical stimulation of PROD electrode locations resulted in orofacial movements consistent with a motor function. Critically, contrary to one of the core dogmas of brain and language, S-M activity occurred bilaterally in the supramarginal gyrus, middle temporal gyrus, superior temporal gyrus, somatosensory cortex, motor cortex, premotor cortex and inferior frontal gyrus (49 electrodes) and was observed in all subjects. Of the 49 S-M sites, 45 sites showed auditory activation during the ‘listen task’ (45 out of 49 electrodes (approximately 92%)), suggesting a role in speech perception. Hemispheric dominance as determined by Wada testing did not correlate with the hemisphere of the electrode placement (χ2 (3) = 0.92, P = 0.34). Importantly, in three subjects with bilateral coverage, S-M activity was present on electrodes in both hemispheres and the likelihood of an electrode being a S-M site did not differ between hemispheres (Fisher’s exact test, P = 0.31). These results demonstrate that S-M activity occurs bilaterally.
Given the evidence for bilateral S-M activity, we performed a series of analyses and experimental manipulations to test the hypothesis that bilateral S-M activity is in fact sensory–motor and represents sensory–motor transformations for speech.
Given the predictions from animal neurophysiology, we tested four subjects as they performed an auditory–motor transformation task (the listen–speak transformation task) that employed two non-words (kig, pob) to examine whether S-M activity has a role in transformations for speech. This task enabled us to hold the sensory and motor components constant while manipulating the transformation process itself in order to measure how the encoding of this content changed depending on how perceptual input was mapped onto production output. The use of non-words instead of words offered other advantages. Non-words enabled us to examine sublexical transformations for speech and could be designed to differ maximally in their articulatory dimensions and their neural representations.
Using direct brain recordings (ECoG) and overt speech, we demonstrate that a sensory–motor system for transforming sublexical speech signals exists bilaterally. Our results are in keeping with models of speech perception that posit bilateral processing but contradict models that posit lateralized sensory–motor transformations. Our results also highlight how S-M activity during perceptual input reflects the transformation of speech sensory input into motor output. We propose that the presence of such transformative activity demonstrates a unified sensory–motor representational interface that links speech-perception- and speech-production-based representations. Such an interface is important during speech articulation, acquisition and self-monitoring. As right hemisphere lesions do not give rise to conduction aphasia, our evidence for bilateral sensory–motor transformations promotes an interesting distinction between speech and language: although sensory–motor transformations are bilateral, the computational system for higher-order language is lateralized. This hypothesis invokes a strong interface between sensory-based speech-perception representations and motor-based speech-production representations and suggests that deficits for conduction aphasia are more abstract and linguistic in nature. We propose that bilateral sublexical transformations could support a unification of perception- and production-based representations into a sensory–motor interface, drawing a distinction between the bilateral perception–production functions of speech and lateralized higher order language processes.
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