Rapid Synaptic Plasticity of Glutamatergic Synapses on Dopamine Neurons in the Ventral Tegmental Area in Response to Acute Amphetamine Injection

Faleiro, Lavina J; Jones, Susan R.; Kauer, Julie A.

doi:10.1038/sj.npp.1300495

Cited by 71 publications

(63 citation statements)

References 54 publications

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“…Electrophysiological studies also support a role for GluR2-lacking receptors in VTA plasticity. Bellone and Luscher (2005) detected a substantial complement of GluR2-lacking receptors in VTA DA neurons of naive rats (P15-P21), which internalized during LTD. Faleiro et al (2004) did not detect GluR2-lacking receptors in VTA DA cells of naive P15-P18 rats. GluR2-lacking receptors were not detected in VTA DA cells of naive mice (Thomas et al, 2000;Bellone and Luscher, 2006) but were added to synapses after cocaine injection (Bellone and Luscher, 2006).…”

Section: Discussionmentioning

confidence: 54%

“…Our studies do not address the mechanism by which D 1 receptor stimulation activates glutamate transmission onto VTA DA neurons, but in vivo and brain slice studies support the hypothesis that D 1 receptors act directly on PFC neurons to increase their excitability and increase glutamate levels in their target regions (Park et al, 2002;Dong and White, 2003). Interestingly, bath application of amphetamine to VTA slices failed to increase the AMPA/NMDA ratio, which could indicate a locus of action outside the VTA (perhaps PFC) but might also indicate a requirement for normal excitatory synaptic transmission, which is absent in the slice preparation (Faleiro et al, 2004). Alternatively, D 1 receptors on glutamate terminals in the VTA may facilitate glutamate release, increasing AMPAR surface and synaptic expression by activity-dependent mechanisms related to those operative in LTP.…”

Section: Discussionmentioning

confidence: 87%

“…An increased AMPA/ NMDA ratio was detected as early as 2 h after amphetamine injection (Faleiro et al, 2004). Regardless of whether rats received a single or multiple cocaine injections, the AMPA/NMDA ratio remained elevated 5 d, but not 10 d after the last exposure (Borgland et al, 2004).…”

Section: Introductionmentioning

confidence: 89%

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Dopamine Alters AMPA Receptor Synaptic Expression and Subunit Composition in Dopamine Neurons of the Ventral Tegmental Area Cultured with Prefrontal Cortex Neurons

Gao¹,

Wolf²

2007

J. Neurosci.

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Excitatory synapses onto dopamine (DA) neurons of the ventral tegmental area (VTA) represent a critical site of psychostimulantinduced synaptic plasticity. This plasticity involves alterations in synaptic strength through AMPA receptor (AMPAR) redistribution. Here, we report an in vitro model for studying regulation of AMPAR trafficking in DA neurons under control conditions and after elevation of DA levels, mimicking cocaine exposure. We used cocultures containing rat VTA neurons and prefrontal cortex (PFC) neurons from enhanced cyan fluorescent protein-expressing mice. In VTA-PFC cocultures, D 1 receptor activation (10 min) increased synaptic and nonsynaptic glutamate receptor subunit 1 (GluR1) and GluR2 surface expression on DA neurons. NMDA or AMPA receptor antagonists blocked this effect, and it was not observed in pure VTA cultures, suggesting that DA agonists acted on D 1 receptors on PFC neurons, altering their excitatory transmission onto VTA DA neurons and, thus, influencing AMPARs. To mimic the longer elevation in extracellular DA levels produced by systemic cocaine, cocultures were incubated with DA for 1 h. Synaptic GluR1 was increased 24 h later, reminiscent of the increased AMPA/NMDA ratio at excitatory synapses onto VTA DA neurons 24 h after cocaine injection (Ungless et al., 2001). In contrast, GluR2 was unchanged. Analysis of colocalization of surface GluR1-3 labeling suggested that control DA neurons express a substantial number of GluR1/2, GluR2/3, and homomeric GluR1 receptors and that the increase in surface AMPARs 24 h after DA exposure may in part reflect increased GluR1/3-containing receptors. These results help define the cellular basis for plasticity underlying the development of behavioral sensitization.

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Section: Discussionmentioning

confidence: 54%

Section: Discussionmentioning

confidence: 87%

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Dopamine Alters AMPA Receptor Synaptic Expression and Subunit Composition in Dopamine Neurons of the Ventral Tegmental Area Cultured with Prefrontal Cortex Neurons

Gao¹,

Wolf²

2007

J. Neurosci.

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“…in vivo for 6 d, and their nucleus accumbens slices were prepared 8-10 d after the last injection. Additionally, a higher AMPAreceptor/ NMDA-receptor ratio at the glutamatergic synapses in the ventral tegmental area (VTA) was associated with higher behavioral sensitization to a single dose of amphetamine in young rats (Faleiro et al 2004). These results indicate that LTP occurred rapidly in the VTA, and with a single amphetamine exposure.…”

Section: Discussionmentioning

confidence: 99%

Memory and psychostimulants: modulation of Pavlovian fear conditioning by amphetamine in C57BL/6 mice

Wood

Anagnostaras

2008

Psychopharmacology

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Rationale and Objectives-With prescriptions of stimulants on the rise, it is important to examine the cognitive effects of low and moderate doses of stimulants, rather than only those typical of addicts.Methods-The present study examined the effects a range of doses (0.005 -8 mg/kg) of damphetamine sulfate on cued and contextual Pavlovian fear conditioning in mice.Results-In agreement with previous research, subjects administered a moderately high dose of amphetamine (8 mg/kg) pre-training, typical of what addicts might take, displayed impaired memory when tested, off-drug. Alternately, subjects injected with a very low dose of amphetamine (0.005, 0.025, or 0.05 mg/kg), pre-training, similar to the therapeutic doses for attention deficit hyperactivity disorder, displayed enhanced memory when tested, off-drug. A control study showed these effects were not due to state-dependent learning.Conclusions-Thus, dose is a critical determinant of the cognitive effects of psychostimulants.

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“…It has been demonstrated that stimulant drugs enhance the ratio of AMPA/NMDA receptor-mediated glutamate neurotransmission in the VTA (Borgland et al, 2004;Boudreau and Wolf, 2005;Faleiro et al, 2004;Saal et al, 2003;Sarti et al, 2007;Ungless et al, 2001), an effect that depends on NMDA receptor neurotransmission at the time of drug treatment (Ungless et al, 2001 …”

Section: Cihr Author Manuscriptmentioning

confidence: 99%

Regulation of netrin-1 receptors by amphetamine in the adult brain

Yetnikoff¹,

Labelle‐Dumais²,

Flores³

2007

Neuroscience

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Netrin-1 is a guidance cue molecule fundamental to the organization of neuronal connectivity during development. Netrin-1 and its receptors, deleted in colorectal cancer (DCC) and UNC-5 homologues (UNC-5), continue to be expressed in the adult brain, although neither their function nor the kinds of events that activate their expression are known. Two lines of evidence suggest a role for netrin-1 in amphetamine-induced dopamine plasticity in the adult. First, DCC is highly expressed by adult dopamine neurons. Second, adult mice with reduced DCC levels do not develop amphetamine-induced behavioral sensitization. To explore the role of netrin-1 in amphetamine-induced plasticity, we examined the effects of sensitizing treatment regimens of amphetamine on DCC and/or UNC-5 protein expression in the adult rat. These treatments produced striking and enduring increases in DCC and UNC-5 expression in the cell body, but not terminal regions, of the mesocorticolimbic dopamine system. Notably, neuroadaptations in the cell body region of mesocorticolimbic dopamine neurons underlie the development of sensitization to the effects of amphetamine. Furthermore, these localized amphetamine-induced changes were prevented by co-treatment with an N-methyl-D-aspartate receptor antagonist, a treatment known to block the development of amphetamine-induced sensitization of behavioral activation, dopamine release and motivated behavior. Using immunohistochemistry, we showed that both DCC and UNC-5 receptors are highly expressed by adult mesocorticolimbic dopamine neurons. These results provide the first evidence that repeated exposure to a stimulant drug such as amphetamine affects netrin-1 receptor expression in the adult brain. Taken together, our findings suggest that changes in netrin-1 receptor expression may play a role in the lasting effects of exposure to amphetamine and other stimulant drugs. Keywords sensitization; DCC; UNC-5; plasticity; dopamine; glutamate Stimulant drugs, such as amphetamine, induce locomotor-activating and rewarding effects by increasing extracellular dopamine (DA) levels in striatal terminal regions. These behavioral and neurochemical effects become sensitized when the drug is administered repeatedly (Stewart and Badiani, 1993;Kalivas and Stewart, 1991;Vezina 2004). Key features of sensitization, including its gradual development and persistence over time, CIHR Author Manuscript CIHR Author Manuscript CIHR Author Manuscriptsuggest underlying alterations in the organization of mesocorticolimbic DA circuitry. Indeed, stimulant-induced modifications in dendritic structure have been identified in midbrain DA perikarya and in striatal and cortical DA terminal regions, suggesting alterations in patterns of synaptic connectivity within these regions (Berlanga et al., 2006;Kolb et al., 2003;Mueller et al., 2006; Kolb, 1997, 1999;Sarti et al., 2007). Although the mechanisms underlying amphetamine-induced plasticity of DA circuitry are unclear, it is known that the development of sensitization depends on (1) ...

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Rapid Synaptic Plasticity of Glutamatergic Synapses on Dopamine Neurons in the Ventral Tegmental Area in Response to Acute Amphetamine Injection

Cited by 71 publications

References 54 publications

Dopamine Alters AMPA Receptor Synaptic Expression and Subunit Composition in Dopamine Neurons of the Ventral Tegmental Area Cultured with Prefrontal Cortex Neurons

Dopamine Alters AMPA Receptor Synaptic Expression and Subunit Composition in Dopamine Neurons of the Ventral Tegmental Area Cultured with Prefrontal Cortex Neurons

Memory and psychostimulants: modulation of Pavlovian fear conditioning by amphetamine in C57BL/6 mice

Regulation of netrin-1 receptors by amphetamine in the adult brain

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