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Volume 16, Number 20,
Issue of October 15, 1996
pp. 6579-6591
Copyright ©1996 Society for Neuroscience
Coordinated Expression of Dopamine Receptors in Neostriatal
Medium Spiny Neurons
Received May 24, 1996; revised July 24, 1996; accepted July 26, 1996.
D. James Surmeier,
Wen-Jie Song, and
Zhen Yan
Department of Anatomy and Neurobiology, College of Medicine,
University of Tennessee, Memphis, Tennessee 38163
In recent years, the distribution of dopamine receptor subtypes
among the principal neurons of the neostriatum has been the subject of
debate. Conventional anatomical and physiological approaches have
yielded starkly different estimates of the extent to which
D1 and D2 class dopamine receptors are
colocalized. One plausible explanation for the discrepancy is that some
dopamine receptors are present in physiologically significant numbers,
but the mRNA for these receptors is not detectable with conventional
techniques. To test this hypothesis, we examined the expression of DA
receptors in individual neostriatal neurons by patch-clamp and
RT-PCR techniques. Because of the strong correlation between peptide
expression and projection site, medium spiny neurons were divided into
three groups on the basis of expression of mRNA for enkephalin (ENK)
and substance P (SP). Neurons expressing detectable levels of SP but
not ENK had abundant mRNA for the D1a receptor. A subset of
these cells (~50%) coexpressed D3 or D4
receptor mRNA. Neurons expressing detectable levels of ENK but not SP
had abundant mRNA for D2 receptor isoforms (short and
long). A subset (10-25%) of these neurons coexpressed D1a
or D1b mRNAs. Neurons coexpressing ENK and SP mRNAs
consistently coexpressed D1a and D2 mRNAs in
relatively high abundance. Functional analysis of neurons expressing
lower abundance mRNAs revealed clear physiological consequences that
could be attributed to these receptors. These results suggest that,
although colocalization of D1a and D2 receptors
is limited, functional D1 and D2 class
receptors are colocalized in nearly one-half of all medium spiny
projection neurons.
Key words:
medium spiny neurons;
single-cell PCR;
voltage clamp;
RT-PCR;
mRNA;
Ca2+ channels;
neuromodulation
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L. Ding and D. J. Perkel
Dopamine Modulates Excitability of Spiny Neurons in the Avian Basal Ganglia
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M. Sato and O. Hikosaka
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S. Yasumoto, E. Tanaka, G. Hattori, H. Maeda, and H. Higashi
Direct and Indirect Actions of Dopamine on the Membrane Potential in Medium Spiny Neurons of the Mouse Neostriatum
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B. L. Waszczak, L. P. Martin, H. E. Finlay, N. Zahr, and J. R. Stellar
Effects of Individual and Concurrent Stimulation of Striatal D1 and D2 Dopamine Receptors on Electrophysiological and Behavioral Output from Rat Basal Ganglia
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J. H. Jhamandas, K. H. Harris, D. MacTavish, and B. S. Jassar
Novel Excitatory Actions of Galanin on Rat Cholinergic Basal Forebrain Neurons: Implications for Its Role in Alzheimer's Disease
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Q. Wang, J. P. Jolly, J. D. Surmeier, B. M. Mullah, M. S. Lidow, C. M. Bergson, and J. D. Robishaw
Differential Dependence of the D1 and D5 Dopamine Receptors on the G Protein gamma 7 Subunit for Activation of Adenylylcyclase
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J. H. Jhamandas, C. Cho, B. Jassar, K. Harris, D. MacTavish, and J. Easaw
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J. Feng, X. Cai, J. Zhao, and Z. Yan
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P. Calabresi, P. Gubellini, B. Picconi, D. Centonze, A. Pisani, P. Bonsi, P. Greengard, R. A. Hipskind, E. Borrelli, and G. Bernardi
Inhibition of Mitochondrial Complex II Induces a Long-Term Potentiation of NMDA-Mediated Synaptic Excitation in the Striatum Requiring Endogenous Dopamine
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D. Herve, C. Le Moine, J.-C. Corvol, L. Belluscio, C. Ledent, A. A. Fienberg, M. Jaber, J.-M. Studler, and J.-A. Girault
G{alpha}olf Levels Are Regulated by Receptor Usage and Control Dopamine and Adenosine Action in the Striatum
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T. Boraud, E. Bezard, B. Bioulac, and C. E. Gross
Dopamine agonist-induced dyskinesias are correlated to both firing pattern and frequency alterations of pallidal neurones in the MPTP-treated monkey
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J. T. Williams, M. J. Christie, and O. Manzoni
Cellular and Synaptic Adaptations Mediating Opioid Dependence
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S. Hernandez-Lopez, T. Tkatch, E. Perez-Garci, E. Galarraga, J. Bargas, H. Hamm, and D. J. Surmeier
D2 Dopamine Receptors in Striatal Medium Spiny Neurons Reduce L-Type Ca2+ Currents and Excitability via a Novel PLC{beta}1-IP3-Calcineurin-Signaling Cascade
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R. R. Metzger, H. M. Haughey, D. G. Wilkins, J. W. Gibb, G. R. Hanson, and A. E. Fleckenstein
Methamphetamine-Induced Rapid Decrease in Dopamine Transporter Function: Role of Dopamine and Hyperthermia
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P. Calabresi, P. Gubellini, D. Centonze, B. Picconi, G. Bernardi, K. Chergui, P. Svenningsson, A. A. Fienberg, and P. Greengard
Dopamine and cAMP-Regulated Phosphoprotein 32 kDa Controls Both Striatal Long-Term Depression and Long-Term Potentiation, Opposing Forms of Synaptic Plasticity
J. Neurosci.,
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R. C. Foehring, P. G. Mermelstein, W.-J. Song, S. Ulrich, and D. J. Surmeier
Unique Properties of R-Type Calcium Currents in Neocortical and Neostriatal Neurons
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G. J. LaHoste, B. L. Henry, and J. F. Marshall
Dopamine D1 Receptors Synergize with D2, But Not D3 or D4, Receptors in the Striatum without the Involvement of Action Potentials
J. Neurosci.,
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K. J. Black, T. Hershey, M. H. Gado, and J. S. Perlmutter
Dopamine D1 Agonist Activates Temporal Lobe Structures in Primates
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O. Hikosaka, Y. Takikawa, and R. Kawagoe
Role of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements
Physiol Rev,
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J. Flores-Hernandez, S. Hernandez, G. L. Snyder, Z. Yan, A. A. Fienberg, S. J. Moss, P. Greengard, and D. J. Surmeier
D1 Dopamine Receptor Activation Reduces GABAA Receptor Currents in Neostriatal Neurons Through a PKA/DARPP-32/PP1 Signaling Cascade
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T. Tkatch, G. Baranauskas, and D. J. Surmeier
Kv4.2 mRNA Abundance and A-Type K+ Current Amplitude Are Linearly Related in Basal Ganglia and Basal Forebrain Neurons
J. Neurosci.,
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W.-J. Song, T. Tkatch, and D. J. Surmeier
Adenosine Receptor Expression and Modulation of Ca2+ Channels in Rat Striatal Cholinergic Interneurons
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M.-Y. Jung and C. Schmauss
Decreased c-fos Responses to Dopamine D1 Receptor Agonist Stimulation in Mice Deficient for D3 Receptors
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M. Roudbaraki, A. Lorsignol, L. Langouche, G. Callewaert, H. Vankelecom, and C. Denef
Target Cells of {gamma}3-Melanocyte-Stimulating Hormone Detected through Intracellular Ca2+ Responses in Immature Rat Pituitary Constitute a Fraction of All Main Pituitary Cell Types, but Mostly Express Multiple Hormone Phenotypes at the Messenger Ribonucleic Acid Level. Refractoriness to Melanocortin-3 Receptor Blockade in the Lacto-Somatotroph Lineage
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P. G. Mermelstein, R. C. Foehring, T. Tkatch, W.-J. Song, G. Baranauskas, and D. J. Surmeier
Properties of Q-Type Calcium Channels in Neostriatal and Cortical Neurons are Correlated with beta Subunit Expression
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G. Torres and J. M. Horowitz
Drugs of Abuse and Brain Gene Expression
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E. V. Gurevich, J. W. Himes, and J. N. Joyce
Developmental Regulation of Expression of the D3 Dopamine Receptor in Rat Nucleus Accumbens and Islands of Calleja
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N. S. Magoski and A. G. M. Bulloch
Dopamine Activates Two Different Receptors to Produce Variability in Sign at an Identified Synapse
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R. Grondin, V. D. Doan, L. Gregoire, and P. J. Bedard
D1 receptor blockade improves L-dopa-induced dyskinesia but worsens parkinsonism in MPTP monkeys
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F. R. Fusco, Q. Chen, W. J. Lamoreaux, G. Figueredo-Cardenas, Y. Jiao, J. A. Coffman, D. J. Surmeier, M. G. Honig, L. R. Carlock, and A. Reiner
Cellular Localization of Huntingtin in Striatal and Cortical Neurons in Rats: Lack of Correlation with Neuronal Vulnerability in Huntington's Disease
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A. E. Stewart, Z. Yan, D. J. Surmeier, and R. C. Foehring
Muscarine Modulates Ca2+ Channel Currents in Rat Sensorimotor Pyramidal Cells Via Two Distinct Pathways
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E. C. Muly III, K. Szigeti, and P. S. Goldman-Rakic
D1 Receptor in Interneurons of Macaque Prefrontal Cortex: Distribution and Subcellular Localization
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J. Drago, P. Padungchaichot, J. Y. F. Wong, A. J. Lawrence, J. F. McManus, S. H. Sumarsono, A. L. Natoli, M. Lakso, N. Wreford, H. Westphal, et al.
Targeted Expression of a Toxin Gene to D1 Dopamine Receptor Neurons by Cre-Mediated Site-Specific Recombination
J. Neurosci.,
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B. L. Waszczak, L. P. Martin, G. J. Greif, and J. E. Freedman
Expression of a dopamine D2 receptor-activated K+ channel on identified striatopallidal and striatonigral neurons
PNAS,
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P. G. Mermelstein, W.-J. Song, T. Tkatch, Z. Yan, and D. J. Surmeier
Inwardly Rectifying Potassium (IRK) Currents Are Correlated with IRK Subunit Expression in Rat Nucleus Accumbens Medium Spiny Neurons
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E. N. Pothos, S. Przedborski, V. Davila, Y. Schmitz, and D. Sulzer
D2-Like Dopamine Autoreceptor Activation Reduces Quantal Size in PC12 Cells
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E. P. Brandon, S. F. Logue, M. R. Adams, M. Qi, S. P. Sullivan, A. M. Matsumoto, D. M. Dorsa, J. M. Wehner, G. S. McKnight, and R. L. Idzerda
Defective Motor Behavior and Neural Gene Expression in RIIbeta -Protein Kinase A Mutant Mice
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W.-J. Song, T. Tkatch, G. Baranauskas, N. Ichinohe, S. T. Kitai, and D. J. Surmeier
Somatodendritic Depolarization-Activated Potassium Currents in Rat Neostriatal Cholinergic Interneurons Are Predominantly of the A Type and Attributable to Coexpression of Kv4.2 and Kv4.1 Subunits
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M. A. Kelly, M. Rubinstein, T. J. Phillips, C. N. Lessov, S. Burkhart-Kasch, G. Zhang, J. R. Bunzow, Y. Fang, G. A. Gerhardt, D. K. Grandy, et al.
Locomotor Activity in D2 Dopamine Receptor-Deficient Mice Is Determined by Gene Dosage, Genetic Background, and Developmental Adaptations
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L. A. Gabel and E. S. Nisenbaum
Biophysical Characterization and Functional Consequences of a Slowly Inactivating Potassium Current in Neostriatal Neurons
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P. J. Blanchet, S. Konitsiotis, and T. N. Chase
Motor Response to a Dopamine D3 Receptor Preferring Agonist Compared to Apomorphine in Levodopa-Primed 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine Monkeys
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