Distinct Temporal Patterns of Human Neural Firing in the Subthalamic Nucleus During Speech and Orofacial Movement
Zahra JourahmadiD, Christopher K. KovachiD, Andrea RohliD, Joel Isaac BergeriD, Kris TjadeniD, Jeremy D.W. GreenleeiD
Abstract
Clinical studies, along with electrophysiological findings, provide evidence that the subthalamic nucleus (STN) contributes to speech production. These studies have reported that the STN encodes diverse aspects of speech, comprising speech motor planning and execution, timing, and linguistic features such as phonetic content. However, none of these studies have included an orofacial non-speech motor task to evaluate speech-specificity of STN activity. Here, we examined the modulation of STN neurons while participants engaged in two speech tasks (sentence repetition and syllable repetition) as well as two non-speech orofacial movement tasks (jaw movement and tongue protrusion) in awake patients with Parkinsons disease undergoing deep brain stimulation implantation surgery. A total of 51 single- and multi-unit neural clusters were captured. A Poisson generalized linear model (GLM) was implemented to understand the temporal dynamics of STN activity. A larger proportion of clusters was modulated during speech (22%) than during orofacial movement (12%) and a substantial subset of STN neural clusters responded to overlapping speech and orofacial tasks (27%). The findings suggest that STN can encode both motor and linguistic aspects of speech production. Graphical abstractThe subthalamic nucleus (STN) shows neural modulation during speech production, a process which requires motor planning, execution, and phonological functions. By comparing STN spiking activity during speech tasks (sentence and syllable repetition) and non-speech orofacial tasks (jaw movement and tongue protrusion), we identified task-specific modulation patterns in STN neurons. The STN contains distinct neural populations engaged during speech and orofacial movements. Among all recorded clusters, 22% responded exclusively to speech, 12% exclusively to orofacial movements, 27% to both, and 39% were non-responsive. We demonstrated that STN activity at single- and multi-unit levels is specific to speech production and is influenced by task-specific motor and linguistic demands, highlighting a role for STN in integrating motor control and speech production. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=108 SRC="FIGDIR/small/693637v1_ufig1.gif" ALT="Figure 1"> View larger version (27K): org.highwire.dtl.DTLVardef@1ec3c60org.highwire.dtl.DTLVardef@6fe46forg.highwire.dtl.DTLVardef@1fe733corg.highwire.dtl.DTLVardef@3f736b_HPS_FORMAT_FIGEXP M_FIG C_FIG
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