Project Summary:
Modulating how we speak is critical for effective communication. The production and modulation of speech, like other behaviors, relies on basal ganglia-thalamocortical networks, not merely on cortical processes. Current knowledge about how the basal ganglia modulate speech, however, is primarily theoretical, due to a lack of empirical data. Theoretical models for speech production, in turn, remain underdeveloped. Notably, no models of speech production include the subthalamic nucleus (STN), a basal ganglia node that has been implicated in multiple cognitive processes relevant to speech production (e.g. action selection/suppression, gain modulation, and motor learning).
Using access to the brain that can only be provided by deep brain stimulation (DBS) surgery, we initiated studies to understand how motor speech information is encoded within the STN-cortical network. We established a novel experimental paradigm to simultaneously record primary motor electrocorticography (ECoG) and STN activity in subjects who are awake and speaking. In our initial project, we discovered separate populations of STN neurons whose inhibition or excitation was selective for either speech planning or production, respectively [1]. We also found that STN population activity tracks with specific articulatory motor features and with vocal gain adjustment [2]. Our discoveries indicate multiple roles for STN activity in speech planning and modulation, consistent with nonhuman primate data that STN neurons are functionally diverse and that the STN is innervated broadly from cortical areas critical for speech production in humans.
We propose to build on our foundational results by exploring how a broader cortical-STN network participates in speech production. Specifically, we have developed a protocol for simultaneous recording of high-density ECoG from the inferior frontal gyrus (IFG), ventral sensorimotor cortex (vSMC), superior temporal gyrus (STG) and the STN. Our preliminary data support the hypothesis that these cortical speech areas communicate with the basal ganglia not only through cortical-striatal direct and indirect pathways, but also through a hyperdirect pathway to STN. These findings include the STG, consistent with evidence for basal ganglia participation in auditory processing. To uncover seminal knowledge about how cortical-basal ganglia dynamics shape speech, we will use intracranial electrophysiology to define the connectivity of speech-related cortex to the STN, while evaluating the role of cortical-STN and cortical-GPi dynamics in two basal ganglia functions critical for speech: motor sequence learning and gain modulation. Our invasive human neuroscience approach is unique in its ability to define, for the first time, a broad cortical-basal ganglia network for modulating speech. Establishing a neurobiological framework for cortical-basal ganglia network control of these processes will represent an order of magnitude change in our understanding of mechanisms for modulating speech, in turn informing how we model the dynamics of other human behaviors modulated by the basal ganglia.
1. Lipski, W. J. et al. Subthalamic Nucleus Neurons Differentially Encode Early and Late Aspects of Speech Production. Journal of Neuroscience 38, 5620–5631 (2018).
2. Chrabaszcz, A. et al. Subthalamic nucleus and sensorimotor cortex activity during speech production. The Journal of Neuroscience 2842–18 (2019). doi:10.1523/JNEUROSCI.2842-18.2019
Research Scientist, Department of Neurosurgery, Massachusetts General Hospital.
Instructor, Harvard Medical School.