Fast oscillatory activity in the anterior cingulate cortex: dopaminergic modulation and effect of perineuronal net loss.

Pascal Steullet,Jan-Harry Cabungcal,Michel Cuã©Nod,Kim Q Do

doi:10.3389/fncel.2014.00244

Pascal Steullet, Jan-Harry Cabungcal + Show 2 more

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https://doi.org/10.3389/fncel.2014.00244

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Abstract

Dopamine release in the prefrontal cortex plays a critical role in cognitive function such as working memory, attention and planning. Dopamine exerts complex modulation on excitability of pyramidal neurons and interneurons, and regulates excitatory and inhibitory synaptic transmission. Because of the complexity of this modulation, it is difficult to fully comprehend the effect of dopamine on neuronal network activity. In this study, we investigated the effect of dopamine on local high-frequency oscillatory neuronal activity (in β band) in slices of the mouse anterior cingulate cortex (ACC). We found that dopamine enhanced the power of these oscillations induced by kainate and carbachol, but did not affect their peak frequency. Activation of D2R and in a lesser degree D1R increased the oscillation power, while activation of D4R had no effect. These high-frequency oscillations in the ACC relied on both phasic inhibitory and excitatory transmission and functional gap junctions. Thus, dopamine released in the ACC promotes high-frequency synchronized local cortical activity which is known to favor information transfer, fast selection and binding of distributed neuronal responses. Finally, the power of these oscillations was significantly enhanced after degradation of the perineuronal nets (PNNs) enwrapping most parvalbumin interneurons. This study provides new insights for a better understanding of the abnormal prefrontal gamma activity in schizophrenia (SZ) patients who display prefrontal anomalies of both the dopaminergic system and the PNNs.

Highlights

Dopamine released in the prefrontal cortex plays a critical role in cognitive function such as working memory, attention and decision making (Seamans and Yang, 2004; Tritsch and Sabatini, 2012)
We investigated whether dopamine can modulate local fast rhythmic neuronal synchronization in slices of the anterior cingulate cortex (ACC), a region of the medial prefrontal cortex richly innervated by dopaminergic neurons (Descarries et al, 1987; Rivera et al, 2008) and affected in several psychiatric conditions (Fountoulakis et al, 2008; Fornito et al, 2009; Minzenberg et al, 2009; Chan et al, 2011; Frodl and Skokauskas, 2012)
In the present study, we show that the power of fast oscillatory activity induced by kainate + carbachol is increased by D2R and D1R activation in ACC slices of mice

Summary

Introduction

Dopamine released in the prefrontal cortex plays a critical role in cognitive function such as working memory, attention and decision making (Seamans and Yang, 2004; Tritsch and Sabatini, 2012). Dopamine receptor activation in the prefrontal cortex can modify synaptic inputs to the cortical network (Gurden et al, 2000) and the local recurrent excitatory synapses (Onn et al, 2006) It can selectively influence the strength of specific outputs to subcortical structures (Gee et al, 2012), increase the inputoutput responses in pyramidal neurons (Thurley et al, 2008), modulate persistent synaptic activity and enhance the signalto-noise ratio (Kroener et al, 2009).

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