Abstract
The nucleus accumbens is thought to contribute to action selection by integrating behaviorally relevant information from multiple regions, including prefrontal cortex. Studies in rodents suggest that information flow to the nucleus accumbens may be regulated via task-dependent oscillatory coupling between regions. During instrumental behavior, local field potentials (LFP) in the rat nucleus accumbens and prefrontal cortex are coupled at delta frequencies (Gruber AJ, Hussain RJ, O'Donnell P. PLoS One 4: e5062, 2009), possibly mediating suppression of afferent input from other areas and thereby supporting cortical control (Calhoon GG, O'Donnell P. Neuron 78: 181–190, 2013). In this report, we demonstrate low-frequency cortico-accumbens coupling in humans, both at rest and during a decision-making task. We recorded LFP from the nucleus accumbens in six epilepsy patients who underwent implantation of deep brain stimulation electrodes. All patients showed significant coherence and phase-synchronization between LFP and surface EEG at delta and low theta frequencies. Although the direction of this coupling as indexed by Granger causality varied between subjects in the resting-state data, all patients showed a cortical drive of the nucleus accumbens during action selection in a decision-making task. In three patients this was accompanied by a significant coherence increase over baseline. Our results suggest that low-frequency cortico-accumbens coupling represents a highly conserved regulatory mechanism for action selection.
Highlights
THE NUCLEUS ACCUMBENS CONTRIBUTES to the selection of goaldirected actions by integrating behaviorally relevant information from the hippocampus, amygdala, and prefrontal cortex, among other areas (Goto and Grace 2008; Grace 2000)
We examined functional and directed connectivity between cortex and the nucleus accumbens in six patients treated with deep brain stimulation (DBS) for drug-resistant epilepsy
Because the connectivity metrics used in this study are sensitive to the number of trials used for analysis, trials in which patients chose the safe option were excluded from the comparison of the four task stages
Summary
THE NUCLEUS ACCUMBENS CONTRIBUTES to the selection of goaldirected actions by integrating behaviorally relevant information from the hippocampus, amygdala, and prefrontal cortex, among other areas (Goto and Grace 2008; Grace 2000). Entrainment of ventral striatal single units to the hippocampal theta rhythm has been associated with combined contextual (spatial) and motivational information (Tabuchi et al 2000; van der Meer and Redish 2011) Together, these results have led to the proposal that theta coupling between the hippocampus and the ventral striatum/nucleus accumbens may regulate how contextual information influences action selection (Grace 2000; Gruber et al 2009a; Pennartz et al 2009). Because theta coherence between the nucleus accumbens core and the hippocampus was simultaneously reduced, the authors suggested that cortico-accumbens coupling may override a hippocampal influence on neuronal excitability in the nucleus accumbens (Calhoon and O’Donnell 2013), thereby promoting behavioral flexibility Translation of these findings to humans has remained speculative, largely because electrophysiological data from the human nucleus accumbens are rare. We could rule out a substantial hippocampal contribution to the observed LFP/EEG coupling in two of the patients who had undergone unilateral resection of the hippocampus before DBS surgery
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