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

Neurosurgery. 2019 Feb 1;84(2):378-387. doi: 10.1093/neuros/nyy027.

Abstract

Background: 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.

MeSH terms

  • Aged
  • Deep Brain Stimulation / instrumentation
  • Deep Brain Stimulation / methods*
  • Female
  • Humans
  • Male
  • Middle Aged
  • Neurons / physiology*
  • Parkinson Disease / physiopathology
  • Parkinson Disease / therapy*
  • Speech / physiology*
  • Subthalamic Nucleus / physiology*