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The Journal of Neuroscience, February 2, 2005, 25(5):1260-1267; doi:10.1523/JNEUROSCI.3436-04.2005

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Cellular/Molecular
Presynaptic D₁ Dopamine Receptors in Primate Prefrontal Cortex: Target-Specific Expression in the Glutamatergic Synapse

Constantinos D. Paspalas and Patricia S. Goldman-Rakic 

Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510

Dopaminergic modulation of glutamate neurotransmission in prefrontal cortex (PFC) microcircuits is commonly perceived as a basis for cognitive operations. Yet it appears that although the control of recurrent excitation between deep-layer prefrontal pyramids may involve presynaptic and postsynaptic D₁ receptor (D₁R) mechanisms, pyramid-to-interneuron communication will engage a postsynaptic D₁R component. The substrate underlying such target-specific neuromodulatory patterns was investigated in the infragranular PFC with immunoelectron microscopy for D₁R and parvalbumin, a marker for fast-spiking interneurons. In addition to their proverbial postsynaptic expression, gold-labeled D₁Rs were distinctly distributed on perisynaptic/extrasynaptic membranes and the axoplasm of 13% of excitatory-like, presumably glutamatergic varicosities. Most importantly, presynaptic D₁Rs were highly specific with regard to the cellular compartment and neurochemical identity of the postsynaptic neuron, being present in spine-targeting varicosities but distinctly absent from those synapsing with parvalbumin profiles often coexpressing D₁Rs. We define therein an axonal D₁ heteroreceptor component, apparently mediating volume neurotransmission, yet strategically positioned to convey target cell-specific modulation of the glutamatergic drive. We also indicate that presynaptic D₁R mechanisms may indeed be associated with recurrent excitation in prefrontal microcircuits, consistent with physiological evidence for a role of these receptors in modulating the persistent activity-profile of neurons essential for working memory.

Key words: dopamine D₁ receptor; glutamate; parvalbumin; presynaptic; prefrontal cortex; recurrent excitation; persistent activity; working memory

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Received Aug 20, 2004; revised December 16, 2004; accepted December 17, 2004.

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