Oscillatory Activity in the Medial Prefrontal Cortex and Nucleus Accumbens Correlates with Impulsivity and Reward Outcome

Abstract

Actions expressed prematurely without regard for their consequences are considered impulsive. Such behaviour is governed by a network of brain regions including the prefrontal cortex (PFC) and nucleus accumbens (NAcb) and is prevalent in disorders including attention deficit hyperactivity disorder (ADHD) and drug addiction. However, little is known of the relationship between neural activity in these regions and specific forms of impulsive behaviour. In the present study we investigated local field potential (LFP) oscillations in distinct sub-regions of the PFC and NAcb on a 5-choice serial reaction time task (5-CSRTT), which measures sustained, spatially-divided visual attention and action restraint. The main findings show that power in gamma frequency (50–60 Hz) LFP oscillations transiently increases in the PFC and NAcb during both the anticipation of a cue signalling the spatial location of a nose-poke response and again following correct responses. Gamma oscillations were coupled to low-frequency delta oscillations in both regions; this coupling strengthened specifically when an error response was made. Theta (7–9 Hz) LFP power in the PFC and NAcb increased during the waiting period and was also related to response outcome. Additionally, both gamma and theta power were significantly affected by upcoming premature responses as rats waited for the visual cue to respond. In a subgroup of rats showing persistently high levels of impulsivity we found that impulsivity was associated with increased error signals following a nose-poke response, as well as reduced signals of previous trial outcome during the waiting period. Collectively, these in-vivo neurophysiological findings further implicate the PFC and NAcb in anticipatory impulsive responses and provide evidence that abnormalities in the encoding of rewarding outcomes may underlie trait-like impulsive behaviour.

The Utility of Impulsive Bias and Altered Decision Making as Predictors of Drug Efficacy and Target Selection: Rethinking Behavioral Screening for Antidepressant Drugs

“…Finally, infusion of the dopamine D 2/3 receptor antagonist sulpiride [N-[(1-ethylpyrrolidin-2-yl)methyl]-2-methoxy-5-sulfamoylbenzamide] into the nucleus accumbens core suppressed the increased impulsivity observed for a mPFC lesion including the anterior cingulate, prelimbic, and IL (Pezze et al, 2009). Thus, this finding and more recent converging evidence support important functional relationships between the ventral PFC and the nucleus accumbens in mediating impulsivity on the 5-CSRTT (Donnelly et al, 2014). While fewer experiments have examined the nucleus accumbens in mediating DRL behavior, these few studies are consistent with findings in the 5-CSRTT literature.…”

Attenuation of cocaine seeking in rats via enhancement of infralimbic cortical activity using stable step-function opsins

“…As the purpose of the in vivo electrophysiological recordings was to demonstrate the effectiveness of SSFO activation in an in vivo preparation in addition to the ex vivo data shown by us and others (Yizhar et al 2011b), the present findings should not be interpreted as indicating that the behavioral effects were due to enhanced gamma rhythm activity. Nonetheless, work by other laboratories suggests that increases in gamma power are linked to a variety of processes including attention, working memory, and action selection, in both primates and rodents (Beshel et al 2007; Donnelly et al 2014; Fries et al 2007; Fries et al 2001; Pesaran et al 2002; Tallon-Baudry et al 1999). …”

A wavelet-based estimator of the degrees of freedom in denoised fMRI time series for probabilistic testing of functional connectivity and brain graphs

“…Wavelet despiking and the analysis methods described here have been tested on, and can also be applied to, fMRI data collected using different acquisition methods, such as short-TR, multi-band and multi-echo data, and on other biological data such as electrophysiological time series. Of note, the algorithm has proven effective at denoising up to 30 min of local field potential data sampled at 500 Hz (Donnelly et al, 2014). Finally, we note that neighboring voxel-wise effective df estimates could be pooled to account for spatial dependence in autocorrelation.…”