Cortical drive of low-frequency oscillations in the human nucleus accumbens during action selection

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.

Perimovement decrease of alpha/beta oscillations in the human nucleus accumbens

“…Recording from neurons in the rat NAcc during a spatial navigation task, van der Meer and Redish (2009a) observed that ensemble firing patterns at a decision point and prior to error correction resembled reward-induced patterns, a finding the authors interpreted as an intrinsically driven expectation signal during decision making. In a recent study of local field potentials (LFPs) from the human NAcc we found a cortical drive of delta oscillations prior to choices in an economic decision making task (Stenner et al 2015a), in line with findings of a similar coupling during instrumental behavior in rodents (Gruber et al 2009). Finally, Patel et al (2012) observed that single-unit activity in the human NAcc predicted the size of a subsequent monetary bet in a computerized card game.…”

“…While Goto and Grace's emphasis of NAcc functions in action selection has inspired much research, particularly in rodents (e.g., Calhoon and O'Donnell 2013; Gruber et al 2009; for a review see Floresco 2015), human research on NAcc function has tended to focus on its role in outcome evaluation (and on an indirect influence on future action selection via an evaluation of past action outcomes; e.g., Pessiglione et al 2006). This focus is also evident across electrophysiological studies of the human NAcc (Cohen et al 2009a, 2009b, 2009c; Lega et al 2011; Stenner et al 2015b; but see Patel et al 2012; Stenner et al 2015a). Here, we extend this view of the human NAcc by showing that a signal that indexes preparation for imminent movement in the motor system is also present in the NAcc.…”

“…Our study is limited by constraints of human invasive electrophysiology, specifically by the clinical diagnoses and pharmacotherapy of participants, and we have previously discussed in detail the limitations of such research (Stenner et al 2015a, 2015b). All patients were treated for pharmacoresistant partial epilepsy.…”

“…We report reanalyses of two separate data sets, recorded during a serial reaction time task and an economic decision making task, respectively (Dürschmid et al 2013; Stenner et al 2015a, 2015b). Both data sets were collected between the second and fifth day after electrode implantation.…”

“…While the relatively small sample sizes in our study limit statistical group-level inference, our data sets offer an excellent opportunity to study the consistency of task-induced modulations across five individual cases in each of the two tasks (see also Stenner et al 2015a, 2015b). To this end, we used a standard nonparametric permutation test across trials, implemented in FieldTrip, which corrects for multiple comparisons across time bins, frequency bins, and channels.…”