Presynaptic D2 dopaminergic receptors mediate inhibition of excitatory synaptic transmission in rat neostriatum

Hsu, Kuei Sen; Huang, Chiung Chun; Cheng, Yang; Gean, Po‐Wu

doi:10.1016/0006-8993(95)00734-8

Cited by 107 publications

(69 citation statements)

References 8 publications

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“…Some laboratories, in fact, reported that DA D2-like receptor activation depressed excitatory synaptic transmission in this brain area, either presynaptically (Hsu et al 1995;Cepeda et al 2001) or postsynaptically (Cepeda et al 1992;Levine et al 1996). In contrast, our group and others found that, at least under control conditions, activation of D2-like receptors caused significant changes neither of glutamate-mediated synaptic potentials (Calabresi et al 1988;Calabresi et al 1992;Calabresi et al 1993;Nicola and Malenka 1998;Pisani et al 2000; present study) nor of exogenous applied AMPA and glutamate (Calabresi et al 1995).…”

Section: Comparison With Other Electrophysiological Studiescontrasting

confidence: 67%

Cocaine and Amphetamine Depress Striatal GABAergic Synaptic Transmission through D2 Dopamine Receptors

Centonze

Picconi

Baunez

et al. 2002

Neuropsychopharmacology

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The striatum is a brain area implicated in the pharmacological action of drugs of abuse. To test the possible involvement of both cocaine and amphetamine in the modulation of synaptic transmission in this nucleus, we coupled whole-cell patch clamp recordings from striatal spiny neurons to the focal stimulation of glutamatergic or GABAergic nerve terminals. We found that neither cocaine (1-600 M) nor amphetamine (0.3-300 M) significantly affected the glutamate-mediated EPSCs recorded from these cells. Conversely, both pharmacological agents depressed GABA-mediated IPSCs in a dose-dependent manner. This effect was mediated by the stimulation of dopamine (DA) D2 receptors since it was prevented by 3 M L-sulpiride (a DA D2-like receptor antagonist), mimicked by the DA D2-like receptor agonist quinpirole (0.3-30 M), and absent in mice lacking DA D2 receptors. A presynaptic mechanism was likely involved in this action since both cocaine and amphetamine depress GABAergic transmission by increasing paired-pulse facilitation. Cocaine and amphetamine failed to affect GABAergic IPSCs after 6-OHDA-induced nigral lesion, indicating that both drugsFollowing psychostimulant administration, markers of brain activity are altered in many areas (Stein and Fuller 1993;Lyons et al. 1996;Breiter et al. 1997), suggesting that the diverse cognitive, emotional, and motor effects of these drugs are caused by the interaction with multiple neuronal systems in the central nervous system. Increasing evidence indicates that not only cortical but also subcortical areas play a role in the cocaine-and amphetamine-mediated effects. In particular, the increased locomotor activity and stereotypy caused by psychostimulants seem to involve specifically the nucleus striatum (Kelly et al. 1975;Amalric and Koob 1993;Berke and Hyman 2000), a structure that receives virtually all the cortical information directed to the basal ganglia (Penney and Young 1983;Albin et al. 1989;McGeorge and Faull 1989;Calabresi et al. 1996 Kaneko et al. 2000). The nucleus striatum also receives profuse dopaminergic innervation from the substantia nigra and has a very high density of D1 and D2 dopamine (DA) receptors but also of D3, D4 and D5 receptors (Mansour and Watson 1995;Surmeier et al. 1996;Bordet et al. 1997;LaHoste et al. 2000). Amphetamine and cocaine cause in the striatum rapid induction of c-fos, a commonly used molecular marker for neuronal activity. Interestingly, this effect is sensitive to dopamine (DA) receptor blockade (Graybiel et al. 1990;Moratalla et al. 1993), suggesting that increased release of DA in the striatum is responsible, at least in part, for the action of these drugs. In this regard, while the full diversity of drug effects is mediated by multiple neurotransmitters acting in multiple brain regions, most drugs abused by humans share the common property of increasing DA release in this brain area (Di Chiara and Imperato 1988; Kuczenshi et al. 1991;Yamamoto and Spanos 1988;Koob et al. 1998;Ito et al. 2000). Cocaine increases DA availability in th...

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Section: Comparison With Other Electrophysiological Studiescontrasting

confidence: 67%

Cocaine and Amphetamine Depress Striatal GABAergic Synaptic Transmission through D2 Dopamine Receptors

Centonze

Picconi

Baunez

et al. 2002

Neuropsychopharmacology

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“…Whereas the D1 receptor is predominantly postsynaptic, at least three functionally distinct D2 receptor "pools" are operative in the striatum. First, D2 receptors on glutamatergic terminals inhibit glutamate release (Hsu et al, 1995;Cepeda et al, 2001); second, D2 receptors on dopaminergic neurons act as release-and synthesis-inhibiting autoreceptors (Skirboll et al, 1979); and third, D2 receptors are expressed postsynaptically on those GABAergic neurons that mediate outflow via the indirect, striatopallidal pathway (Harrison et al, 1992). Notably, the two pools of presynaptic D2 receptors exert opposite effects on the activity of the GABAergic neurons; agonist binding to D2 receptors on dopaminergic terminals will reduce dopamine release that will indirectly increase cortico-striatal drive and GABAergic cellular activity (Calabresi et al, 1993;Gubellini et al, 2002), whereas agonist binding to D2 receptors on glutamate terminals will reduce glutamate release, and hence reduce GABAergic cellular activity.…”

Section: Discussionmentioning

confidence: 99%

“…Activation of D2 family (D2, D3, and D4) receptors located postsynaptically is associated with either a decrease or no effect on NMDA and non-NMDA receptor responsivity (Cepeda et al, 1993;Cepeda and Levine, 1998). However, evidence suggests that DA inhibits glutamate release via activation of presynaptic D2 heteroceptors on cortico-striatal glutamatergic afferents (Hsu et al, 1995); consequently, D2 receptor knockout mice exhibit increased striatal glutamatergic transmission (Cepeda et al, 2001).…”

mentioning

confidence: 99%

Differential Regulation of the Endocannabinoids Anandamide and 2-Arachidonylglycerol within the Limbic Forebrain by Dopamine Receptor Activity

Patel

Rademacher²,

Hillard³

2003

J Pharmacol Exp Ther

142

100

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Glutamatergic synaptic transmission within the striatum and prefrontal cortex regulates the neuronal synthesis of endocannabinoids. Because a primary role of dopamine is to modulate this excitatory transmission, we tested the hypothesis that dopaminergic transmission modulates endocannabinoid content in the limbic forebrain. Liquid chromatography/mass spectrometry was used to determine endogenous anandamide and 2-arachidonylglycerol (2-AG) contents within the limbic forebrain of mice after pharmacological manipulation of dopaminergic transmission. Increasing synaptic dopamine concentrations with methylphenidate significantly and dose dependently decreased both anandamide and 2-AG content. The selective dopamine reuptake inhibitor 1-[2-[bis(4-fluorophenyl)methoxy]ethyl]-4-(3-phenylpropyl)piperazine (GBR 12909) also significantly decreased anandamide and tended to decrease 2-AG content. The D1 receptor antagonist R-(ϩ)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine (SCH 23390) increased and the D1 receptor agonist 2,3,4,5-tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine (SKF 33939) decreased anandamide content. 2-AG content was unaffected by SCH 23390 but was significantly increased by the D2 receptor antagonist eticlopride, which had no effect on anandamide content. The D2 agonist quinpirole had a biphasic effect on anandamide content with low, autoreceptor-preferring doses increasing anandamide and higher doses decreasing it back toward control. Quinpirole did not significantly affect 2-AG content. Together, these data indicate that endogenous dopamine exerts a differential, net suppressive effect upon anandamide and 2-AG content via activation of D1 and D2 receptors, respectively. These data are consistent with the hypothesis that modulation of endocannabinoid content by dopamine is secondary to changes in glutamatergic transmission, and they provide a pharmacological framework for the rational development of endocannabinoid-based therapeutic interventions for dopamine-related neuropsychiatric disorders.

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“…Previous studies have demonstrated that glutamate release from corticostriatal fibers is dependent on striatal dopamine and may be regulated by D2 receptors located on corticostriatal terminals (Maura et al, 1988;Garcia-Munoz et al, 1991;Calabresi et al, 1993;O'Donnell and Grace, 1994;Hsu et al, 1995;FloresHernandez et al, 1997;Cepeda et al, 2001;Tang et al, 2001;Bamford et al, 2004). To determine whether D2-like receptors regulate corticostriatal activity in DD mice, we examined the effect of the D2-like antagonist sulpiride and the D2-like agonist quinpirole on corticostriatal FM1-43 unloading.…”

Section: D2-like Receptor Agonists Regulate Corticostriatal Destaininmentioning

confidence: 99%

“…Although this anatomical configuration suggests that dopamine has a direct modulatory effect on cortical signaling (Arbuthnott et al, 1998), the role of dopamine in presynaptic modification of corticostriatal afferents has been controversial because of the extraordinary complexity of MSN innervation (Akopian and Walsh, 2002) and the challenges inherent in using postsynaptic recordings to determine alterations in presynaptic activity (Van der Kloot, 1991;Sulzer and Pothos, 2000). Electron microscopy (Fisher et al, 1994;Sesack et al, 1994;Wang and Pickel, 2002) and electrophysiology (Calabresi et al, 1993;O'Donnell and Grace, 1994;Hsu et al, 1995;Flores-Hernandez et al, 1997;Cepeda et al, 2001;Tang et al, 2001;Bamford et al, 2004) studies, however, have supported the concept that dopamine directly regulates glutamate release from corticostriatal terminals by stimulating D2 receptors located on a subpopulation of cortical afferents, providing a mechanism for dampening critical cortical signals (Bamford et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Dopamine Modulates Release from Corticostriatal Terminals

et al. 2004

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Normal striatal function is dependent on the availability of synaptic dopamine to modulate neurotransmission. Within the striatum, excitatory inputs from cortical glutamatergic neurons and modulatory inputs from midbrain dopamine neurons converge onto dendritic spines of medium spiny neurons. In addition to dopamine receptors on medium spiny neurons, D2 receptors are also present on corticostriatal terminals, where they act to dampen striatal excitation. To determine the effect of dopamine depletion on corticostriatal activity, we used the styryl dye FM1-43 in combination with multiphoton confocal microscopy in slice preparations from dopaminedeficient (DD) and reserpine-treated mice. The activity-dependent release of FM1-43 out of corticostriatal terminals allows a measure of kinetics quantified by the halftime decay of fluorescence intensity. In DD, reserpine-treated, and control mice, exposure to the D2-like receptor agonist quinpirole revealed modulation of corticostriatal kinetics with depression of FM1-43 destaining. In DD and reserpinetreated mice, quinpirole decreased destaining to a greater extent, and at a lower dose, consistent with hypersensitive corticostriatal D2 receptors. Compared with controls, slices from DD mice did not react to amphetamine or to cocaine with dopamine-releasing striatal stimulation unless the animals were pretreated with L-3,4-dihydroxyphenylalanine (L-dopa). Electron microscopy and immunogold labeling for glutamate terminals within the striatum demonstrated that the observed differences in kinetics of corticostriatal terminals in DD mice were not attributable to aberrant cytoarchitecture or glutamate density. Microdialysis revealed that basal extracellular striatal glutamate was normal in DD mice. These data indicate that dopamine deficiency results in morphologically normal corticostriatal terminals with hypersensitive D2 receptors.

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Presynaptic D2 dopaminergic receptors mediate inhibition of excitatory synaptic transmission in rat neostriatum

Cited by 107 publications

References 8 publications

Cocaine and Amphetamine Depress Striatal GABAergic Synaptic Transmission through D2 Dopamine Receptors

Cocaine and Amphetamine Depress Striatal GABAergic Synaptic Transmission through D2 Dopamine Receptors

Differential Regulation of the Endocannabinoids Anandamide and 2-Arachidonylglycerol within the Limbic Forebrain by Dopamine Receptor Activity

Dopamine Modulates Release from Corticostriatal Terminals

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