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Review
.2007 Apr;191(3):609-25.
doi: 10.1007/s00213-006-0527-8. Epub 2006 Nov 4.

The ability of the mesocortical dopamine system to operate in distinct temporal modes

Affiliations
Review

The ability of the mesocortical dopamine system to operate in distinct temporal modes

Christopher C Lapish et al. Psychopharmacology (Berl).2007 Apr.

Abstract

Background: This review discusses evidence that cells in the mesocortical dopamine (DA) system influence information processing in target areas across three distinct temporal domains.

Discussions: Phasic bursting of midbrain DA neurons may provide temporally precise information about the mismatch between expected and actual rewards (prediction errors) that has been hypothesized to serve as a learning signal in efferent regions. However, because DA acts as a relatively slow modulator of cortical neurotransmission, it is unclear whether DA can indeed act to precisely transmit prediction errors to prefrontal cortex (PFC). In light of recent physiological and anatomical evidence, we propose that corelease of glutamate from DA and/or non-DA neurons in the VTA could serve to transmit this temporally precise signal. In contrast, DA acts in a protracted manner to provide spatially and temporally diffuse modulation of PFC pyramidal neurons and interneurons. This modulation occurs first via a relatively rapid depolarization of fast-spiking interneurons that acts on the order of seconds. This is followed by a more protracted modulation of a variety of other ionic currents on timescales of minutes to hours, which may bias the manner in which cortical networks process information. However, the prolonged actions of DA may be curtailed by counteracting influences, which likely include opposing actions at D1 and D2-like receptors that have been shown to be time- and concentration-dependent. In this way, the mesocortical DA system optimizes the characteristics of glutamate, GABA, and DA neurotransmission both within the midbrain and cortex to communicate temporally precise information and to modulate network activity patterns on prolonged timescales.

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Figures

Fig. 1
Fig. 1
Orders of magnitude in the observed time course following dopamine (DA) application or VTA stimulation.a A very fast EPSP–IPSP sequence can be recorded in prefrontal cortical cells after stimulation of the VTA in-vivo. The EPSP is evoked with a latency on the order of milliseconds and is thought to be the result of corelease of glutamate from dopamine cells in the VTA.b Depolarization of a fast-spiking interneuron by DA in the prefrontal cortex in vitro. Local pressure application of DA leads to depolarization and repolarization of the membrane potential that seems to follow the diffusion of the drug in the slice on the timescale of seconds (Kroener and Seamans, unpublished observations).c Modulation of a variety of intrinsic and synaptic currents by DA has been shown to occur over minutes and hours both in vivo and in vitro. Activation of D1- and D2-type receptors occurs in both pyramidal cells and interneurons, adding to DA’s ability to modulate network behavior. The time course and direction of some of the effects indicated in the diagram have been shown to be concentration- and receptor-specific. It is assumed that in vivo the very long lasting effects that have been reported in experimental settings can be curtailed by fluctuating levels of extracellular DA and opposing effects at the different DA receptors that result from it. See text for details
Fig. 2
Fig. 2
Anatomy of a dopaminergic VTA neuron, illustrating the distal dendritic location from which the axon can originate. Composite confocal images of a VTA neuron recorded in a coronal brain slice of a transgenic mouse expressing green fluorescent protein under the control of the TH gene promoter (TH-GFP+). The green cell was filled with a red dye (Alexa 594) during the recording, resulting in a yellow signal in the merged image. Theinsert represents a magnified view of the white square in the main picture. Thearrow points where the axon (on theright) branches off the dendrite
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