Directed Communication between Nucleus Accumbens and Neocortex in Humans Is Differentially Supported by Synchronization in the Theta and Alpha Band

PLoS One. 2015 Sep 22;10(9):e0138685. doi: 10.1371/journal.pone.0138685. eCollection 2015.

Abstract

Here, we report evidence for oscillatory bi-directional interactions between the nucleus accumbens and the neocortex in humans. Six patients performed a demanding covert visual attention task while we simultaneously recorded brain activity from deep-brain electrodes implanted in the nucleus accumbens and the surface electroencephalogram (EEG). Both theta and alpha oscillations were strongly coherent with the frontal and parietal EEG during the task. Theta-band coherence increased during processing of the visual stimuli. Granger causality analysis revealed that the nucleus accumbens was communicating with the neocortex primarily in the theta-band, while the cortex was communicating the nucleus accumbens in the alpha-band. These data are consistent with a model, in which theta- and alpha-band oscillations serve dissociable roles: Prior to stimulus processing, the cortex might suppress ongoing processing in the nucleus accumbens by modulating alpha-band activity. Subsequently, upon stimulus presentation, theta oscillations might facilitate the active exchange of stimulus information from the nucleus accumbens to the cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Algorithms
  • Alpha Rhythm / physiology*
  • Analysis of Variance
  • Brain Mapping / methods
  • Cortical Synchronization / physiology*
  • Depressive Disorder / physiopathology
  • Electrodes, Implanted
  • Electroencephalography / instrumentation
  • Electroencephalography / methods
  • Female
  • Humans
  • Male
  • Middle Aged
  • Models, Neurological
  • Neocortex / physiopathology*
  • Neural Pathways / physiology
  • Nucleus Accumbens / physiopathology*
  • Obsessive-Compulsive Disorder / physiopathology
  • Photic Stimulation
  • Substance-Related Disorders / physiopathology
  • Theta Rhythm / physiology*
  • Young Adult

Grant support

This work is supported by the research program "The healthy brain" funded by the Netherlands Initiative Brain and Cognition (NIHC), a part of the Organization for Scientific Research (NWO) under grant numbers 056-14-011 (O.J.) and 056-14-012 (D.D.), a VICI grant under number 453-09-002 (O.J.). R.C. is supported by a James McDonnell Scholar Award. The DBS intervention was supported by an unrestricted investigator-initiated research grant by Medtronic Inc., which provided the devices used.