Subthalamic Nucleus and Sensorimotor Cortex Activity During Speech Production

• Published in: The Journal of neuroscience Vol. 39; no. 14; pp. 2698 - 2708
• Main Authors: Chrabaszcz, Anna, Neumann, Wolf-Julian, Stretcu, Otilia, Lipski, Witold J, Bush, Alan, Dastolfo-Hromack, Christina A, Wang, Dengyu, Crammond, Donald J, Shaiman, Susan, Dickey, Michael W, Holt, Lori L, Turner, Robert S, Fiez, Julie A, Richardson, R Mark
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 03-04-2019
• Subjects: Aged; Brain; Brain Mapping - methods; Coding; Cortex (somatosensory); Cortex (temporal); Electrical stimuli; Electrocorticography - methods; Electrodes; Empathy; Female; Humans; Implantation; Jaw; Larynx; Male; Middle Aged; Movement disorders; Neurodegenerative diseases; Parkinson's disease; Phonemes; Photic Stimulation - methods; Sensorimotor Cortex - physiology; Solitary tract nucleus; Speech; Speech - physiology; Subthalamic nucleus; Subthalamic Nucleus - physiology; Tongue; Vocal tract; electrocorticography; Parkinson's disease; sensorimotor cortex; speech; subthalamic nucleus; deep brain stimulation
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.2842-18.2019

The sensorimotor cortex is somatotopically organized to represent the vocal tract articulators such as lips, tongue, larynx, and jaw. How speech and articulatory features are encoded at the subcortical level, however, remains largely unknown. We analyzed LFP recordings from the subthalamic nucleus (STN) and simultaneous electrocorticography recordings from the sensorimotor cortex of 11 human subjects (1 female) with Parkinson's disease during implantation of deep-brain stimulation (DBS) electrodes while they read aloud three-phoneme words. The initial phonemes involved either articulation primarily with the tongue (coronal consonants) or the lips (labial consonants). We observed significant increases in high-gamma (60-150 Hz) power in both the STN and the sensorimotor cortex that began before speech onset and persisted for the duration of speech articulation. As expected from previous reports, in the sensorimotor cortex, the primary articulators involved in the production of the initial consonants were topographically represented by high-gamma activity. We found that STN high-gamma activity also demonstrated specificity for the primary articulator, although no clear topography was observed. In general, subthalamic high-gamma activity varied along the ventral-dorsal trajectory of the electrodes, with greater high-gamma power recorded in the dorsal locations of the STN. Interestingly, the majority of significant articulator-discriminative activity in the STN occurred before that in sensorimotor cortex. These results demonstrate that articulator-specific speech information is contained within high-gamma activity of the STN, but with different spatial and temporal organization compared with similar information encoded in the sensorimotor cortex.
Clinical and electrophysiological evidence suggest that the subthalamic nucleus (STN) is involved in speech; however, this important basal ganglia node is ignored in current models of speech production. We previously showed that STN neurons differentially encode early and late aspects of speech production, but no previous studies have examined subthalamic functional organization for speech articulators. Using simultaneous LFP recordings from the sensorimotor cortex and the STN in patients with Parkinson's disease undergoing deep-brain stimulation surgery, we discovered that STN high-gamma activity tracks speech production at the level of vocal tract articulators before the onset of vocalization and often before related cortical encoding.