Serotonin microinfusion into the ventral tegmental area increases accumbens dopamine release

Guan, Xiaojiao; McBride, William J.

doi:10.1016/0361-9230(89)90198-6

Cited by 177 publications

(82 citation statements)

References 42 publications

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“…This mechanism is consistent with recent studies demonstrating increased striatal dopamine levels after acute administration of the 5-HT releaser and uptake inhibitor fenfluramine (Smith et al 1997) and chronic administration of the 5-HT uptake inhibitor citalopram (Tiihonen et al 1996) in normal subjects as assessed by PET and [ 11 C]raclopride. In animal studies, local application of 5-HT or 5-HT agonists by means of microdialysis was also reported to increase extracellular DA in the striatum (Benloucif and Galloway 1991;Benloucif et al 1993;Bonhomme et al 1995) and nucleus accumbens (Guan and McBride 1989;Parson and Justice 1993;Boulenguez et al 1996). However, there is a minority of studies reporting an inhibitory influence of serotonergic stimulation on striatal dopamine concentration (Dewey et al 1995;Kapur and Remington 1996).…”

Section: Discussionmentioning

confidence: 99%

“…For example, there is evidence that serotonin may inhibit (de Belleroche and Bradford 1980;Ennis et al 1981;Westfall and Tittermary 1982;Blandina et al 1988) as well as stimulate DA release in the striatum (Benloucif et al 1993;West and Galloway 1996;De Deurwaerdere et al 1997). Similarly, local application of 5-HT or 5-HT agonists have been shown to reduce (de Belleroche and Gardiner 1982) and facilitate dopamine efflux in the nucleus accumbens (Guan and McBride 1989;Parson and Justice 1993). In respect to the 5-HT 2 receptor agonist properties of psilocybin, it is of particular note that 3,4-methylenedioxymethamphetamine (MDMA), a potent 5-HT releasing agent, has been shown to increase impulse-mediated striatal dopamine release through 5-HT 2 receptor activation (Schmidt et al 1992;Palfreyman et al 1993;Schmidt et al 1994;Yamamoto et al 1995;Gudelsky and Nash 1996).…”

Section: The Modulating Effects Of Serotonin On Dopamine Neurotransmimentioning

confidence: 99%

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5-HT Modulation of Dopamine Release in Basal Ganglia in Psilocybin-Induced Psychosis in Man—A PET Study with [11C]raclopride

Vollenweider

1999

Neuropsychopharmacology

261

138

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The modulating effects of serotonin on dopamine neurotransmission are not well understood, particularly in acute psychotic states. Positron emission tomography was used to examine the effect of psilocybin on the in vivo binding of [ 11 C]raclopride to D 2 -dopamine receptors in the striatum in healthy volunteers after placebo and a psychotomimetic dose of psilocybin (n ϭ 7). Psilocybin is a potent indoleamine hallucinogen and a mixed 5-HTPsilocybin, a potent indoleamine hallucinogen and 5-HT receptor stimulating agent, has been reported to produce a psychosis-like syndrome in man resembling the first manifestation of schizophrenia in certain respects [for review see (Fischman 1983;Gouzoulis-Mayfrank et al. 1998)]. Particularly, ego-disorders (Rüm-mele and Gnirss 1961;Vollenweider et al. 1997), affective changes (Rümmele and Gnirss 1961), loosened associations (Spitzer et al. 1996) and perceptual alterations commonly seen in psilocybin-induced psychosis are also observed in incipient acute schizophrenic stages (Bowers and Freedman 1966;Heimann, 1986;Gouzoulis et al. 1994). In support of these suggested clinical similarities, we recently found that psilocybin produced a marked prefrontal and anterior cingulate activation in normal subjects comparable to the hyperfrontal pattern observed in some (Cleghorn et al. 1989;Ebmeier et al. 1993Ebmeier et al. , 1995Catafau et al. 1994 1994;Ebmeier et al. 1995;Sabri et al. 1997) but not all (Andreasen et al. 1992;Buchsbaum et al. 1992;Liddle et al. 1992;Siegel et al. 1993) acute schizophrenic patients. A number of functional animal studies have suggested that indoleamine (psilocybin, LSD) and phenylethylamine (DOI, mescaline) hallucinogens produce their psychotomimetic effects primarily through excessive stimulation of 5-HT, and 5-HT 2A receptors in particular (McKenna et al. 1989;Pierce and Peroutka 1989;Aghajanian 1994;Sipes and Geyer 1994;Padich et al. 1996). This assumption was corroborated in a recent human study demonstrating that the psychotomimetic effects of psilocybin can be blocked dose-dependently by pretreatment with the preferential 5-HT 2A receptor antagonist ketanserin (Vollenweider et al. 1998). However, pretreatment with the D 2 -antagonist haloperidol also reduces some of the positive symptoms of psilocybin psychosis. This raises the possibility that symptoms of psilocybin are secondary responses to increased dopaminergic transmission (Vollenweider et al. 1998).Hence, a contribution of the dopamine systems to the effects of psilocybin, presumably through a serotonindopamine interaction, cannot be ruled out. Functional interactions between central serotonin (5-HT) and dopamine (DA) systems have been well documented. Electrophysiological, biochemical, and behavioral evidence suggests that the ascending serotonergic pathways from the medial and dorsal raphe modulate or control the function of the mesolimbic and mesostriatal dopamine systems (Joyce 1993;Zazpe et al. 1994;Kapur and Remington 1996). The modulating effect of serotonin on striatal dopamine release...

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Section: Discussionmentioning

confidence: 99%

Section: The Modulating Effects Of Serotonin On Dopamine Neurotransmimentioning

confidence: 99%

5-HT Modulation of Dopamine Release in Basal Ganglia in Psilocybin-Induced Psychosis in Man—A PET Study with [11C]raclopride

Vollenweider

1999

Neuropsychopharmacology

261

138

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“…An effect of 5-HT within both the VTA and the NAC may contribute to the observed increase of accumbal DA release. Although the presence of 5-HT 3 receptors in the ventral midbrain is controversial (Perry, 1990;, intra-V TA injection of 5-HT and 5-HT 3 agonists enhance, respectively, accumbal DA release (Guan and McBride, 1989) and locomotor activity (Mylecharane, 1996). This latter effect is blocked by the intra-V TA administration of ondansetron (Mylecharane, 1996).…”

Section: Discussionmentioning

confidence: 99%

Opposite Change ofIn VivoDopamine Release in the Rat Nucleus Accumbens and Striatum That Follows Electrical Stimulation of Dorsal Raphe Nucleus: Role of 5-HT₃Receptors

1998

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In the present study we investigate, using in vivo microdialysis, the involvement of central 5-HT 3 receptors in the effect of dorsal raphe nucleus (DRN) electrical stimulation on dopamine (DA), 3,4-dihydroxyphenylacetic acid (DOPAC), and 5-hydroxyindole-3-acetic acid (5-HIAA) extracellular levels monitored in the nucleus accumbens and the striatum of halothane-anesthetized rats. DRN stimulation (300 A, 1 msec at 3, 5, 10, and 20 Hz for 15 min) induced a frequencydependent increase of accumbal DA release and a concomitant reduction of DA release in the ipsilateral striatum at 20 Hz. In both structures DOPAC and 5-HIAA dialysate contents were enhanced in a frequency-dependent manner. Central serotonin (5-HT) depletion, induced by intra-raphe injections of 5,7-dihydroxytryptamine neurotoxin, abolished the effect of 20 Hz DRN stimulation on DA, DOPAC, and 5-HIAA extracellular levels in both regions. The 5-HT synthesis inhibitor parachlorophenylalanine (3 ϫ 400 mg/kg, i.p., for 3 d), although preventing the effect on DA release, failed to modify significantly the effect of 20 Hz DRN stimulation on DOPAC and 5-HIAA outflow in both structures. Ondansetron (0.1 and 1 mg/kg) and (S)-zacopride (0.1 mg/kg), two 5-HT 3 antagonists, significantly impaired the increase of accumbal DA release induced by 20 Hz DRN stimulation but did not affect either the decrease of striatal DA release or the increase in DOPAC outflow in both structures. These results indicate that an enhancement of central 5-HT transmission induced by DRN stimulation differentially affects striatal and accumbal DA release and that endogenous 5-HT, via its action on 5-HT 3 receptors, exerts a facilitatory control restricted to the mesoaccumbal DA pathway.

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“…In areas such as the NAcc where dopamine release is under tonic inhibitory control, the effect of glutamate receptor blockade on dopamine release is thought to involve a reduction of the activity of GABAergic interneurons in the VTA that, in turn, modulate the activity of dopaminergic cells [13]. This idea is supported by evidence that administration of GABA agonists into the VTA can decrease extracellular dopamine levels within the NAcc [22,50] and that rats will self-administer glutamate antagonists or GABA receptor antagonists, but not GABA agonists [27] into the VTA. GABA modulation of dopamine function also is supported by evidence that systemic administration of the dopamine antagonist sulpiride blocks the rewarding effects of GABA receptor blockade [12].…”

Section: Introductionmentioning

confidence: 99%

Ventral tegmental area involvement in pair bonding in male prairie voles

Curtis

Wang

2005

Physiology & Behavior

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Dopamine is known to play a critical role in social attachment in monogamous voles. However, little is known about the neurochemical regulation of central dopamine release during pair bond formation. Here we examine the effects on partner preference formation in male prairie voles of neurochemical manipulations in the ventral tegmental area (VTA), a major source of dopamine to brain regions implicated in pair bonding. Administration of NBQX, an AMPA receptor antagonist, or bicuculline, a GABA receptor antagonist, into the VTA induced partner preferences within 6 h in the absence of mating. We also found that, after unilateral administration of NBQX into the VTA, neuronal activation, as indicated by the expression of the immediate early gene c-fos, was decreased in the nucleus accumbens, prefrontal cortex, and medial amygdala, but was unchanged in the lateral septum and in a control region, the arcuate nucleus. These results confirm a role for the VTA in partner preference formation in monogamous voles and extend the list of neurochemicals important in pair bonding to include glutamate and GABA. D

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Serotonin microinfusion into the ventral tegmental area increases accumbens dopamine release

Cited by 177 publications

References 42 publications

5-HT Modulation of Dopamine Release in Basal Ganglia in Psilocybin-Induced Psychosis in Man—A PET Study with [11C]raclopride

5-HT Modulation of Dopamine Release in Basal Ganglia in Psilocybin-Induced Psychosis in Man—A PET Study with [11C]raclopride

Opposite Change ofIn VivoDopamine Release in the Rat Nucleus Accumbens and Striatum That Follows Electrical Stimulation of Dorsal Raphe Nucleus: Role of 5-HT₃Receptors

Ventral tegmental area involvement in pair bonding in male prairie voles

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Serotonin microinfusion into the ventral tegmental area increases accumbens dopamine release

Cited by 177 publications

References 42 publications

5-HT Modulation of Dopamine Release in Basal Ganglia in Psilocybin-Induced Psychosis in Man—A PET Study with [11C]raclopride

5-HT Modulation of Dopamine Release in Basal Ganglia in Psilocybin-Induced Psychosis in Man—A PET Study with [11C]raclopride

Opposite Change ofIn VivoDopamine Release in the Rat Nucleus Accumbens and Striatum That Follows Electrical Stimulation of Dorsal Raphe Nucleus: Role of 5-HT3Receptors

Ventral tegmental area involvement in pair bonding in male prairie voles

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Opposite Change ofIn VivoDopamine Release in the Rat Nucleus Accumbens and Striatum That Follows Electrical Stimulation of Dorsal Raphe Nucleus: Role of 5-HT₃Receptors