Dopamine drives left-hemispheric lateralization of neural networks during human speech

J Comp Neurol. 2018 Apr 1;526(5):920-931. doi: 10.1002/cne.24375. Epub 2017 Dec 21.

Abstract

Although the concept of left-hemispheric lateralization of neural processes during speech production has been known since the times of Broca, its physiological underpinnings still remain elusive. We sought to assess the modulatory influences of a major neurotransmitter, dopamine, on hemispheric lateralization during real-life speaking using a multimodal analysis of functional MRI, intracranial EEG recordings, and large-scale neural population simulations based on diffusion-weighted MRI. We demonstrate that speech-induced phasic dopamine release into the dorsal striatum and speech motor cortex exerts direct modulation of neuronal activity in these regions and drives left-hemispheric lateralization of speech production network. Dopamine-induced lateralization of functional activity and networks during speaking is not dependent on lateralization of structural nigro-striatal and nigro-motocortical pathways. Our findings provide the first mechanistic explanation for left-hemispheric lateralization of human speech that is due to left-lateralized dopaminergic modulation of brain activity and functional networks.

Keywords: fMRI; hemispheric lateralization; iEEG; neural modeling; speech production.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Aged
  • Brain Mapping*
  • Broca Area* / diagnostic imaging
  • Broca Area* / metabolism
  • Broca Area* / physiology
  • Dopamine / metabolism*
  • Electroencephalography
  • Female
  • Functional Laterality / physiology*
  • Humans
  • Imaging, Three-Dimensional
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Motor Cortex / drug effects
  • Motor Cortex / physiology
  • Speech / physiology*

Substances

  • Dopamine