Goal: Summary of aims  

Aim 1 - uses stimulation and functional connectivity measures to map the cortical-STN speech network.

Aim 2 - in parallel, probes proposed basal ganglia functions relevant to speech, by simultaneously recording neural activity and speech acoustics during an auditory repetition tasks that employs the Lombard Effect to selectively perturb speech production.

Aim 3 - The resulting data will inform modifications to current models of speech production, which subsequently will be tested with cue and response-locked intraoperative stimulation.

Study population and setting:

Actions are not mediated solely by cortical processes but rely on communication within basal ganglia- thalamocortical loops. Speech is one example, although how the basal ganglia participate in this uniquely human behavior is not clear, due to a lack of empirical data. For instance, the leading computational model of speech production ignores the hyperdirect cortical pathway to the subthalamic nucleus (STN), a basal ganglia node that has been implicated in multiple cognitive processes relevant to speech production (e.g. action selection and suppression, behavioral switching, gain modulation, motor learning). Recognizing that deep brain stimulation (DBS) surgery offers the only opportunity to directly measure neural activity in the human basal ganglia, we initiated studies to understand how motor and linguistic speech information is encoded within the STN-sensorimotor cortical network. We established a novel experimental paradigm, where electrocorticography (ECoG) is recorded simultaneously with STN single unit activity and local field potentials (LFP), during DBS surgery in which patients are awake and speaking. We discovered that STN neuron activity is dynamic during speech production, exhibiting behaviorally-selective inhibition and excitation of separate populations of neurons. At the population level, we found that STN activity tracks with specific articulatory motor features and with gain adjustment in articulatory movements. In addition, our data suggest a role for the STN in speech planning, in that STN activity appears to be modulated prior to speech onset. These findings led us to expand ECoG coverage to additionally record from areas involved in speech perception (superior temporal gyrus) and planning (inferior frontal gyrus). Given the evidence in nonhuman primates for an auditory basal ganglia-thalamocortical loop and the known hyperdirect projections from broad areas of frontal cortex to the STN, we propose that hyperdirect pathways from both speech perception and speech planning areas of cortex project to the STN and contribute to speech control. Supporting this idea, we have recorded evoked potentials after STN stimulation that are consistent with antidromic activation not only in sensorimotor cortex, but also from the inferior frontal gyrus (IFG) and superior temporal gyrus (STG). Our principal hypothesis is that interactions between the STN and functionally distinct cortical regions contribute to multiple aspects of speech, at the levels of perception, planning and modulation.

Data generated:

Publications

• Accurate Deep Brain Stimulation Lead Placement Concurrent With Research Electrocorticography.
  Kons Z, Hadanny A, Bush A, Nanda P. Herrington TM, Richardson RM. Operative Neurosurgery. 2022.
• Lateralized and region-specific thalamic processing of lexical status during reading aloud.
  Wang D, Lipski WJ, Bush A, Chrabaszcz A, Dastolfo-Hromack C, Dickey MW, Fiez JA, Richardson RM. JNeurosci. 2022.
• Hyperdirect connectivity of opercular speech networks to the subthalamic nucleus.
  Jorge A, Lipski WJ, Wang D, Crammond DJ, Turner RS, Richardson RM. Cell Reports. 2022.
• Differentiation of speech-induced artifacts from physiological high gamma activity in intracranial recordings.
  Bush A, Chrabaszcz A, Peterson V, Saravanan V, Dastolfo-Hromack C, Lipski WJ, Richardson RM. NeuroImage. 2021.
• Articulatory Gain Predicts Motor Cortex and Subthalamic Nucleus Activity During Speech.
  C Dastolfo-Hromack, A Bush, A Chrabaszcz, A Alhourani, W Lipski, D Wang, D J Crammond, S Shaiman, M W Dickey, L L Holt, R S Turner, J A Fiez, RM Richardson. Cerebral Cortex. 2021.
• Simultaneously recorded subthalamic and cortical LFPs reveal different lexicality effects during reading aloud.
  Chrabaszcz A, Wang D, Lipski WJ, Bush A, Crammond DJ, Shaiman S, Dickey MW, Holt LL, Turner RS, Fiez JA, Richardson RM. J Neurolinguistics. 2021.
• ECoG During Deep Brain Stimulation Surgery: Safety Experience From 4 Centers Within the NINDS Research Opportunities in Human Consortium
  Sisterson ND, Carlson AA, Rutishauser U, Mamelak AN, Flagg M, Pouratian N, Salimpour Y, Anderson WS, Richardson RM. Neurosurgery. 2021.

Resources:

Website

Brain Modulation Lab

Linkedin URL

https://www.linkedin.com/in/mark-richardson-a901011a/

Twitter URL

https://twitter.com/RMarkRichardson

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