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Presynaptic D1Dopamine Receptors in Primate Prefrontal Cortex: Target-Specific Expression in the Glutamatergic Synapse

Paspalas, Constantinos D., Goldman-Rakic, Patricia S.·2005·The Journal of Neuroscience
DOI 10.1523/jneurosci.3436-04.2005
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Abstract

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 D 1 receptor (D 1 R) mechanisms, pyramid-to-interneuron communication will engage a postsynaptic D 1 R component. The substrate underlying such target-specific neuromodulatory patterns was investigated in the infragranular PFC with immunoelectron microscopy for D 1 R and parvalbumin, a marker for fast-spiking interneurons. In addition to their proverbial postsynaptic expression, gold-labeled D 1 Rs were distinctly distributed on perisynaptic/extrasynaptic membranes and the axoplasm of 13% of excitatory-like, presumably glutamatergic varicosities. Most importantly, presynaptic D 1 Rs 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 D 1 Rs. We define therein an axonal D 1 heteroreceptor component, apparently mediating volume neurotransmission, yet strategically positioned to convey target cell-specific modulation of the glutamatergic drive. We also indicate that presynaptic D 1 R 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.

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Figure 2 D 1 Rs in axons and adjoining structures. A , Two varicosities [axon 1 (ax1) and ax2] and two dendritic spines (sp) with well defined spine apparata (asterisks) are juxtaposed but show no synaptic interaction in this plain of section; the junctional specialization in frame is an adherens junction. Ax1 and one spine display D 1 R-nanogold labeling. B-E , Typically, the D 1 R + boutonsestablishasymmetricsynapticcontacts(betweenarrowheads)withD 1 R + orD 1 R -spines. In D , note the D 1 R + synaptic pair bordering an immunonegative pair. Presynaptic D 1 Rs are distributed on extrasynaptic membranes (arrows in E ) or perisynaptically often within the peripheral active zone of the excitatory synapse (arrows in C ). This is generally accompanied by axoplasmic labeling. Scale bars: A , B , 400 nm; C-E , 200 nm.
Figure 2 D 1 Rs in axons and adjoining structures. A , Two varicosities [axon 1 (ax1) and ax2] and two dendritic spines (sp) with well defined spine apparata (asterisks) are juxtaposed but show no synaptic interaction in this plain of section; the junctional specialization in frame is an adherens junction. Ax1 and one spine display D 1 R-nanogold labeling. B-E , Typically, the D 1 R + boutonsestablishasymmetricsynapticcontacts(betweenarrowheads)withD 1 R + orD 1 R -spines. In D , note the D 1 R + synaptic pair bordering an immunonegative pair. Presynaptic D 1 Rs are distributed on extrasynaptic membranes (arrows in E ) or perisynaptically often within the peripheral active zone of the excitatory synapse (arrows in C ). This is generally accompanied by axoplasmic labeling. Scale bars: A , B , 400 nm; C-E , 200 nm.CC-BY-NC-SA · From the PDF
Figure 3 D 1 Rs in PV (diffuse precipitate) cellular profiles. A , PV perikarya display D 1 Rs in association with endomembranes, whereas only a fraction is expressed on the plasmalemma (arrow). B , Similarly, in PV dendrites (den), D 1 Rs may appear intracellularly and on nonsynaptic membranes (arrows). Note a second D 1 R-immunoreactive dendrite shown to the bottom right in B . C , A PV varicosity (double arrowheads point to synaptic vesicles) lies next to an e-l bouton [axon 1 (ax1)] forming a synapse with perforated postsynaptic density (between arrowheads). Unlike the PV axon, ax1 and neighboring ax2 show perisynaptic and extrasynaptic D 1 R labeling (arrows). Two other synaptic pairs also express D 1 Rs. mit, Mitochondrion; lys, lysosome; sp, spine. Scale bars, 400 nm.
Figure 3 D 1 Rs in PV (diffuse precipitate) cellular profiles. A , PV perikarya display D 1 Rs in association with endomembranes, whereas only a fraction is expressed on the plasmalemma (arrow). B , Similarly, in PV dendrites (den), D 1 Rs may appear intracellularly and on nonsynaptic membranes (arrows). Note a second D 1 R-immunoreactive dendrite shown to the bottom right in B . C , A PV varicosity (double arrowheads point to synaptic vesicles) lies next to an e-l bouton [axon 1 (ax1)] forming a synapse with perforated postsynaptic density (between arrowheads). Unlike the PV axon, ax1 and neighboring ax2 show perisynaptic and extrasynaptic D 1 R labeling (arrows). Two other synaptic pairs also express D 1 Rs. mit, Mitochondrion; lys, lysosome; sp, spine. Scale bars, 400 nm.CC-BY-NC-SA · From the PDF
Figure 5 Synopsis of the various relationships between pyramidal neurons and PV interneurons, as well as D 1 R expression patterns in the infragranular PFC. It should be explicitly stated that the schema depicts a simplistic view of complex and certainly not fully understood principles of neocortical organization. For clarity, two pyramids ( A , B ) and two PV cells ( C , D ) are illustrated. D 1 R-immunoreactive spines, axon varicosities, and perinuclear Golgi complexes appear in red, and, likewise, red patches below the cell surface represent somatic and dendritic D 1 Rs. Synaptic and extrasynaptic (curved arrows) DAergic input from the ventral tegmental area (VTA) is shown in orange. Thalamic afferents, in brown, cross the infragranular cortex and terminate in layers IV/deepIII. Blue lines represent intrinsic, associational, and callosal corticocortical afferents; they may or may not furnish D 1 R + e-l varicosities (see Discussion) and thus should be potentially regarded as an integral part of the circuitry (only local axon collaterals are illustrated here). Neuron A establishes axospinous and axodendritic synapses with cells B and C, respectively, which exemplify the pattern of target-specific expression of presynaptic D 1 heteroreceptors. Almost 80% of such axospinous contacts may express bothpresynapticandpostsynapticD 1 Rs. PV interneurons provide synaptic input to the perisomatic region (C-to-B synapses) or the axon initial segment (D-to-B synapses) of pyramidal neurons. The lower discontinuous portion of one PV axon (that could originate from a neuron other than C) participates in a rare multipartite arrangement with a pyramidal axon where both express D 1 Rs (Fig. 4 D ). In effect, DA would modulate all four neurons postsynaptically, via direct synapses (to neurons B and C) or via volume neurotransmission.
Figure 5 Synopsis of the various relationships between pyramidal neurons and PV interneurons, as well as D 1 R expression patterns in the infragranular PFC. It should be explicitly stated that the schema depicts a simplistic view of complex and certainly not fully understood principles of neocortical organization. For clarity, two pyramids ( A , B ) and two PV cells ( C , D ) are illustrated. D 1 R-immunoreactive spines, axon varicosities, and perinuclear Golgi complexes appear in red, and, likewise, red patches below the cell surface represent somatic and dendritic D 1 Rs. Synaptic and extrasynaptic (curved arrows) DAergic input from the ventral tegmental area (VTA) is shown in orange. Thalamic afferents, in brown, cross the infragranular cortex and terminate in layers IV/deepIII. Blue lines represent intrinsic, associational, and callosal corticocortical afferents; they may or may not furnish D 1 R + e-l varicosities (see Discussion) and thus should be potentially regarded as an integral part of the circuitry (only local axon collaterals are illustrated here). Neuron A establishes axospinous and axodendritic synapses with cells B and C, respectively, which exemplify the pattern of target-specific expression of presynaptic D 1 heteroreceptors. Almost 80% of such axospinous contacts may express bothpresynapticandpostsynapticD 1 Rs. PV interneurons provide synaptic input to the perisomatic region (C-to-B synapses) or the axon initial segment (D-to-B synapses) of pyramidal neurons. The lower discontinuous portion of one PV axon (that could originate from a neuron other than C) participates in a rare multipartite arrangement with a pyramidal axon where both express D 1 Rs (Fig. 4 D ). In effect, DA would modulate all four neurons postsynaptically, via direct synapses (to neurons B and C) or via volume neurotransmission.CC-BY-NC-SA · From the PDF

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Metadata

Authors
Paspalas, C. D., & Goldman-Rakic, P. S.
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2005-02-02
Volume
25
Issue
5
Pages
1260-1267
ISSN
  • 0270-6474
  • 1529-2401
DOI
10.1523/jneurosci.3436-04.2005
Cited by
94
References
9
Language
en
Licence
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)

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