Dopamine Gates Visual Signals in Monkey Prefrontal Cortex Neurons

Maximilian Stalter,Stephanie Westendorff,Andreas Nieder

doi:10.1016/j.celrep.2019.11.082

Maximilian Stalter, Stephanie Westendorff + Show 1 more

Open Access

https://doi.org/10.1016/j.celrep.2019.11.082

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Journal: Cell Reports	Publication Date: Jan 1, 2020
Citations: 18	License type: cc-by

Affiliation: University of Tübingen

Abstract

The neurotransmitter dopamine, which acts via the D1-like receptor (D1R) and D2-like receptor (D2R) family, may play an important role in gating sensory information to the prefrontal cortex (PFC). We tested this hypothesis in awake macaques and recorded visual motion-direction tuning functions of single PFC neurons. Using micro-iontophoretic drug application combined with single-unit recordings, we simulated receptor-specific dopaminergic input to the PFC and explored cellular gating mechanisms. We find that stimulating D1Rs, and particularly D2Rs, enhances the single-neuron and populationcoding quality in PFC neurons. D2R stimulation causes aclear increase of the neurons' responses to the preferred motion direction and a decrease to the non-preferred motion direction, thus enhancing neuronal signal-to-noise ratio. Neither D1R nor D2R stimulation had any impact on the neurons' tuning sharpness. These results elucidate the mechanisms of how receptor-specific dopamine effects can act as a gating signal that enables privileged access of sensory information to PFC circuits.

Highlights

The primate prefrontal cortex (PFC) is considered to act as the brain’s central executive (Miller and Cohen, 2001)
Dopamine binds to five different dopamine receptors that fall into two main receptor types (Seamans and Yang, 2004), the D1-like receptor (D1R) family, with subtypes D1 and D5, and the D2-like receptor (D2R), with subtypes D2, D3, and D4
In agreement with the overall hypothesis that dopamine in PFC provides a gating signal to enable privileged access of sensory information to PFC circuits (Braver and Cohen, 1999; Cohen et al, 2002; Ott and Nieder, 2019), we found that pharmacological stimulation of dopamine receptors enhanced the sensory sensitivity of PFC neurons tuned to visual motion direction

Summary

Introduction

The primate prefrontal cortex (PFC) is considered to act as the brain’s central executive (Miller and Cohen, 2001). It is engaged in various cognitive control processes, such as categorization (Freedman et al, 2001; Nieder et al, 2002), working memory (Funahashi et al, 1989; Jacob and Nieder, 2014; Rainer et al, 1998a), rule switching (Eiselt and Nieder, 2013; Vallentin et al, 2012; Wallis et al, 2001), and decision making (Kim and Shadlen, 1999; Merten and Nieder, 2012). Dopamine binds to five different dopamine receptors that fall into two main receptor types (Seamans and Yang, 2004), the D1-like receptor (D1R) family, with subtypes D1 and D5, and the D2R, with subtypes D2, D3, and D4

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