Neuronal Encoding of Speech Features in the Human Thalamus in Parkinson’s Disease and Essential Tremor Patients

Neurosurgery 94:307–316, 2024

The human thalamus is known, from stimulation studies and functional imaging, to participate in high-level language tasks. The goal of this study is to find whether and how speech features, in particular, vowel phonemes, are encoded in the neuronal activity of the thalamus, and specifically of the left ventralis intermediate nucleus (Vim), during speech production, perception, and imagery.

METHODS: In this cross-sectional study, we intraoperatively recorded single neuron activity in the left Vim of eight neurosurgical patients with Parkinson’s disease (PD) (n = 4) or essential tremor (n = 4) undergoing implantation of deep brain stimulation (n = 3) or radiofrequency lesioning (n = 5) while patients articulated the five monophthongal vowel sounds.

RESULTS: In this article, we report that single neurons in the left Vim encode individual vowel phonemes mainly during speech production but also during perception and imagery. They mainly use one of two encoding schemes: broad or sharp tuning, with a similar percentage of units each. Sinusoidal tuning has been demonstrated in almost half of the broadly tuned units. Patients with PD had a lower percentage of speech-related units in each aspect of speech (production, perception, and imagery), a significantly lower percentage of broadly tuned units, and significantly lower median firing rates during speech production and perception, but significantly higher rates during imagery, than patients with essential tremor.

CONCLUSION: The results suggest that the left Vim uses mixed encoding schemes for speech features. Our findings explain, at the single neuron level, why deep brain stimulation and radiofrequency lesioning of the left Vim are likely to cause speech side effects. Moreover, they may indicate that speech-related units in the left Vim of patients with PD may be degraded even in the subclinical phase.

Degradation of Neuronal Encoding of Speech in the Subthalamic Nucleus in Parkinson’s Disease

Neurosurgery 84:378–387, 2019

Most of the patients with Parkinson’s disease suffer from speech disorders characterized mainly by dysarthria and hypophonia.

OBJECTIVE: To understand the deterioration of speech in the course of Parkinson’s disease.

METHODS: We intraoperatively recorded single neuron activity in the subthalamic nucleus of 18 neurosurgical patients with Parkinson’s disease undergoing implantation of deep brain stimulator while patients articulated 5 vowel sounds.

RESULTS: Here, we report that single subthalamic neurons encode individual vowel phonemes and employ 1 of 2 encoding schemes: broad or sharp tuning. Broadly tuned units respond to all examined phonemes, each with a different firing rate, whereas sharply tuned ones are specific to 1 to 2 phonemes. We then show that in comparison with patients without speech deficits, the spiking activity in patients with speech disorders was lower during speech production, overt or imagined, but not during perception. However, patients with speech disorders employed a larger percentage of the neurons for the aforementioned tasks. Whereas the lower firing rates affect mainly sharply tuned units, the extra units used a broad tuning encoding scheme.

CONCLUSION: Our findings suggest mechanisms of neuronal degradation due to Parkinsonian speech disorders and their possible compensation. As impairment in sharply tuned units may be compensated by broadly tuned ones, the proposed compensation model appears to be suboptimal, lending support to the persistence of speech disorders in the course of the disease.