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

Jörn M Horschig; Ruud Smolders; Mathilde Bonnefond; Jan-Mathijs Schoffelen; Pepijn van den Munckhof; P Richard Schuurman; Roshan Cools; Damiaan Denys; Ole Jensen

doi:10.1371/journal.pone.0138685

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.

Authors

Jörn M Horschig¹, Ruud Smolders², Mathilde Bonnefond¹, Jan-Mathijs Schoffelen³, Pepijn van den Munckhof⁴, P Richard Schuurman⁴, Roshan Cools⁵, Damiaan Denys⁶, Ole Jensen¹

Affiliations

¹ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands.
² Department of Psychiatry, Academic Medical Center, Amsterdam, The Netherlands.
³ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands; Max-Planck Institute for Psycholinguistics, Nijmegen, The Netherlands.
⁴ Department of Neurosurgery, Academic Medical Center, Amsterdam, The Netherlands.
⁵ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands; Department of Psychiatry, Radboud University Medical Center, Nijmegen, The Netherlands.
⁶ Department of Psychiatry, Academic Medical Center, Amsterdam, The Netherlands; The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Science, Amsterdam, The Netherlands.

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

Grants and funding

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.