Human Sensorimotor Cortex Control of Directly Measured Vocal Tract Movements during Vowel Production

Abstract

During speech production, we make vocal tract movements with remarkable precision and speed. Our understanding of how the human brain achieves such proficient control is limited, in part due to the challenge of simultaneously acquiring high-resolution neural recordings and detailed vocal tract measurements. To overcome this challenge, we combined ultrasound and video monitoring of the supralaryngeal articulators (lips, jaw, and tongue) with electrocorticographic recordings from the cortical surface of 4 subjects (3 female, 1 male) to investigate how neural activity in the ventral sensory-motor cortex (vSMC) relates to measured articulator movement kinematics (position, speed, velocity, acceleration) during the production of English vowels. We found that high-gamma activity at many individual vSMC electrodes strongly encoded the kinematics of one or more articulators, but less so for vowel formants and vowel identity. Neural population decoding methods further revealed the structure of kinematic features that distinguish vowels. Encoding of articulator kinematics was sparsely distributed across time and primarily occurred during the time of vowel onset and offset. In contrast, encoding was low during the steady-state portion of the vowel, despite sustained neural activity at some electrodes. Significant representations were found for all kinematic parameters, but speed was the most robust. These findings enabled by direct vocal tract monitoring demonstrate novel insights into the representation of articulatory kinematic parameters encoded in the vSMC during speech production. Speaking requires precise control and coordination of the vocal tract articulators (lips, jaw, and tongue). Despite the impressive proficiency with which humans move these articulators during speech production, our understanding of how the brain achieves such control is rudimentary, in part because the movements themselves are difficult to observe. By simultaneously measuring speech movements and the neural activity that gives rise to them, we demonstrate how neural activity in sensorimotor cortex produces complex, coordinated movements of the vocal tract.

Subthalamic nucleus and sensorimotor cortex activity during speech production

“…For the sensorimotor cortex, we found that 30% of recording sites revealed either lips-preferred or tongue-preferred activity, which had a topographic distribution: the electrodes located more dorsally on the sensorimotor cortex produced a greater high gamma power for the articulation of lips consonants while the electrodes that were located more ventrally yielded a greater high gamma power for tongue consonants. Thus, our results appear to recapitulate the expected dorsoventral layout for lips and tongue representations within the primary motor and sensory cortices (Penfield and Boldrey, 1937;Bouchard et al, 2013;Breshears et al, 2015;Chartier et al, 2018;Conant et al, 2018). We found that the density of articulator-discriminative observations closely aligned with the consonant onset in acoustic speech production.…”

“…In contrast to the STN, the magnitude of cortical high gamma activity was not significantly different across recording locations. Given that the cortical recordings were confined to the orofacial segment of the sensorimotor cortex and the evidence of overlapping speech-related activation in the precentral and postcentral gyri (Cheung et al, 2016;Conant et al, 2018), this lack of spatial differentiation in the cortical high gamma activity is expected.…”

“…Functional imaging (fMRI) studies generally provide corroborating evidence for the somatotopic cortical representation of the vocal tract effectors, among other body parts, albeit with a varying degree of overlap among individuals (Lotze et al, 2000;Hesselmann et al, 2004;Pulvermüller et al, 2006;Brown, Ngan, and Liotti, 2007;Meier et al, 2008;Takai, Brown, and Liotti, 2010;Carey et al, 2017). Recently, ECoG studies have elaborated the notion of cortical articulatory somatotopy by revealing differentiated neural representations for fine-grained phonetic features and complex kinematics underlying speech articulation (Bouchard et al, 2013;Bouchard & Chang, 2014;Mugler et al, 2014;Lotte et al, 2015;Bouchard et al, 2016;Cheung et al, 2016;Ramsey et al, 2017;Chartier et al, 2018;Conant et al, 2018).…”

Singing training predicts increased insula connectivity with speech and respiratory sensorimotor areas at rest

“…This interpretation is supported by the specific functional involvement of the co-activated areas, which process visceral and somatosensory information underlying voluntary respiratory, laryngeal, and articulatory sensorimotor control (Banzett et al, 2000;Bouchard et al, 2013;Brown et al, 2008;Conant et al, 2014;Conant et al, 2018;Khalsa et al, 2009;Pfenning et al, 2014). Vocalization related movements are accompanied by proprioceptive, kinesthetic, and interoceptive consequences, which in turn are integrated with the motor system to guide song and speech production (Bernardi et al, 2015;Gozaine and Clark, 2005;Nasir and Ostry, 2006;Simonyan and Horwitz, 2011;Smotherman, 2007;Tremblay et al, 2003;Wyke, 1974).…”

Learning long temporal sequences in spiking networks by multiplexing neural oscillations

“…Finally, our task of speech production was restricted to learning a spectrogram of the target signal. This simplified task did not account for the neural control of articulatory speech kinetics, likely involving the ventral sensory-motor cortex (54, 55).…”