Cortical-Basal Ganglia Speech Networks

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