Hippocampal and striatal responses during motor learning are modulated by prefrontal cortex stimulation

Neuroimage. 2021 Aug 15:237:118158. doi: 10.1016/j.neuroimage.2021.118158. Epub 2021 May 12.

Abstract

While it is widely accepted that motor sequence learning (MSL) is supported by a prefrontal-mediated interaction between hippocampal and striatal networks, it remains unknown whether the functional responses of these networks can be modulated in humans with targeted experimental interventions. The present proof-of-concept study employed a multimodal neuroimaging approach, including functional magnetic resonance (MR) imaging and MR spectroscopy, to investigate whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex can modulate responses in the hippocampus and the basal ganglia during motor learning. Our results indicate that while stimulation did not modulate motor performance nor task-related brain activity, it influenced connectivity patterns within hippocampo-frontal and striatal networks. Stimulation also altered the relationship between the levels of gamma-aminobutyric acid (GABA) in the stimulated prefrontal cortex and learning-related changes in both activity and connectivity in fronto-striato-hippocampal networks. This study provides the first experimental evidence, to the best of our knowledge, that brain stimulation can alter motor learning-related functional responses in the striatum and hippocampus.

Keywords: GABA; Hippocampus; Motor learning; Prefrontal cortex; Striatum; Theta-burst stimulation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Caudate Nucleus / diagnostic imaging
  • Caudate Nucleus / metabolism
  • Caudate Nucleus / physiology*
  • Connectome*
  • Evoked Potentials, Motor / physiology*
  • Hippocampus / diagnostic imaging
  • Hippocampus / metabolism
  • Hippocampus / physiology*
  • Humans
  • Magnetic Resonance Imaging
  • Magnetic Resonance Spectroscopy
  • Motor Activity / physiology*
  • Prefrontal Cortex / diagnostic imaging
  • Prefrontal Cortex / metabolism
  • Prefrontal Cortex / physiology*
  • Proof of Concept Study
  • Psychomotor Performance / physiology*
  • Serial Learning / physiology*
  • Transcranial Magnetic Stimulation*
  • Young Adult
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • gamma-Aminobutyric Acid