Psychostimulants Induce Low-Frequency Oscillations in the Firing Activity of Dopamine Neurons

Shi, Wei‐Xing; Pun, Chen-Lun; Zhou, Yan

doi:10.1038/sj.npp.1300534

Cited by 60 publications

(102 citation statements)

References 33 publications

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“…Treatment with the DA antagonists used in our study should also prevent a slowly developing inhibition, which is presumably mediated via DA autoreceptors. In fact, instead of inhibition, cocaine increased the activity of presumed DA VTA neurons in anesthetized animals treated with raclopride, a selective D2 antagonist (Shi et al, 2004). In contrast to rapid, transient excitations produced by cocaine at low dose in our experiments, this increase was tonic and much weaker despite the much higher drug dose.…”

Section: Sensory Effects Of IV Cocaine On Different Subgroups Of Vta contrasting

confidence: 62%

“…Cocaine-induced excitations of LS VTA neurons seen in this study appear to contrast to mainly inhibitory responses of presumed DA neurons to iv cocaine reported in the SNc and VTA in anesthetized animals (Einhorn et al, 1988;Hinerth et al, 2000;Pitts and Marwah, 1987;Shi et al, 2004). However, this latter effect was much slower (latencies 20-40 s), much more prolonged (10-20 min), relatively weak both on SNc and VTA neurons (ED 50 8.8 and 1.2 mg/ kg, respectively; Hinerth et al, 2000), and blocked by D2 antagonists (Zhou et al, 2006), suggesting its central pharmacological determination.…”

Section: Sensory Effects Of IV Cocaine On Different Subgroups Of Vta contrasting

confidence: 47%

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Sensory effects of intravenous cocaine on dopamine and non-dopamine ventral tegmental area neurons

Brown

Kiyatkin

2008

Brain Research

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Intravenous (iv) cocaine mimics salient somato-sensory stimuli in their ability to induce rapid physiological effects, which appear to involve its action on peripherally located neural elements and fast neural transmission via somato-sensory pathways. To further clarify this mechanism, single-unit recording with fine glass electrodes was used in awake rats to examine responses of ventral tegmental area (VTA) neurons, both presumed dopamine (DA) and non-DA, to iv cocaine and tail-press, a typical somato-sensory stimulus. To exclude the contribution of DA mechanisms to the observed neuronal responses to sensory stimuli and cocaine, recordings were conducted during full DA receptor blockade (SCH23390+eticloptide).Iv cocaine (0.25 mg/kg delivered over 10 s) induces significant excitations of ~63% of long-spike (presumed DA) and ~70% of short-spike (presumed non-DA) VTA neurons. In both subgroups, neuronal excitations occurred with short latencies (4-8 s), peaked at 10-20 s (30-40% increase over baseline) and disappeared at 30-40 s after the injection onset. Most long-(67%) and short-spike (89%) VTA neurons also showed phasic responses to tail-press (5-s). All responsive long-spike cells were excited by tail-press; excitations were very rapid (peak at 1 s) and strong (100% rate increase over baseline) but brief (2-3 s). In contrast, both excitations (60%) and inhibitions (29%) were seen in short-spike cells. These responses were also rapid and transient, but excitations of short-spike units were more prolonged and sustained (10-15 s) than in long-spike cells.These data suggest that in awake animals iv cocaine, like somato-sensory stimuli, rapidly and transiently excites VTA neurons of different subtypes. Therefore, along with direct action on specific brain substrates, central effects of cocaine may occur via indirect mechanism, involving peripheral neural elements, visceral sensory nerves and rapid neural transmission. Via this mechanism, cocaine, like somato-sensory stimuli, can rapidly activate DA neurons and induce phasic DA release, creating the conditions for DA accumulation by a later occurring and prolonged direct inhibiting action on DA uptake. By providing a rapid neural signal and triggering transient neural activation, such a peripherally driven action might play a crucial role in the sensory effects of COC, thus contributing to learning and development of drug-taking behavior.

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Section: Sensory Effects Of IV Cocaine On Different Subgroups Of Vta contrasting

confidence: 62%

Section: Sensory Effects Of IV Cocaine On Different Subgroups Of Vta contrasting

confidence: 47%

Sensory effects of intravenous cocaine on dopamine and non-dopamine ventral tegmental area neurons

Brown

Kiyatkin

2008

Brain Research

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“…This non-DA-mediated effect, expressed as an increase in both firing rate and a slow oscillation (SO) in firing pattern, is most evident when the DA-mediated feedback mechanisms are blocked. Results further show that the excitatory effect of D-amphetamine depends on forebrain inputs to DA neurons and requires activation of adrenergic a1 receptors (Shi et al, 2000b(Shi et al, , 2004.…”

Section: Introductionmentioning

confidence: 75%

“…The resulting increase in extracellular DA, in turn, activates various feedback mechanisms, leading to an inhibition of DA cell firing and thus a decrease in impulse-dependent DA release (Bunney et al, 1973;Groves et al, 1975;Bunney and Aghajanian, 1978;Wang, 1981;Shi et al, 2000a). We have recently shown that D-amphetamine also has an excitatory influence on DA neurons through a non-DA mechanism (Shi et al, 2000b(Shi et al, , 2004. This non-DA-mediated effect, expressed as an increase in both firing rate and a slow oscillation (SO) in firing pattern, is most evident when the DA-mediated feedback mechanisms are blocked.…”

Section: Introductionmentioning

confidence: 99%

“…All current antipsychotic drugs have D2 antagonist properties. Blockade of D2-like receptors not only removes the D2-mediated feedback inhibition, but also enhances the a1-mediated excitation of DA neurons (Shi et al, 2000b(Shi et al, , 2004. Both effects promote impulse-dependent DA release, thus counteracting the direct blocking effect of the drug on DA receptors.…”

Section: Introductionmentioning

confidence: 99%

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Clozapine Blocks D-Amphetamine-Induced Excitation of Dopamine Neurons in the Ventral Tegmental Area

Shi

Zhang

Pun

et al. 2007

Neuropsychopharmacol

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Current antipsychotic drugs are thought to inhibit central dopamine (DA) transmission by blocking DA receptors. Here, we provide evidence that the atypical antipsychotic drug clozapine may produce part of its effect by inhibiting a subset of excitatory inputs to DA neurons. Thus, in chloral hydrate-anesthetized rats, systemic administration of D-amphetamine produced two opposing effects on DA neurons in the ventral tegmental area. Under control conditions, D-amphetamine inhibited the firing of the cell through D2-like receptors. When D2-like receptors were blocked by raclopride, D-amphetamine excited DA neurons, instead of producing no effect. The excitation, expressed as an increase in firing rate and a slow oscillation in firing pattern, was suppressed by the adrenergic a1 receptor antagonist prazosin, suggesting an involvement of a1 receptors. In rats pretreated with the typical antipsychotic drug haloperidol, D-amphetamine also excited DA neurons. However, when given after clozapine, D-amphetamine produced no significant effects. The failure of D-amphetamine to produce an excitation is not due to an incomplete blockade of D2-like receptors by clozapine because co-treatment with clozapine and raclopride also failed to enable the excitatory effect of D-amphetamine. The suggestion that clozapine inhibits the excitatory effect of D-amphetamine is further supported by the finding that clozapine, given after D-amphetamine, reliably reversed D-amphetamine-induced excitation in raclopride-treated rats. Thus, different from raclopride and haloperidol, clozapine may inhibit DA transmission through two additive mechanisms: blockade of DA receptors and inhibition of an amphetamine-sensitive, excitatory pathway that innervates DA neurons.

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Oscillatory firing of dopamine neurons: Differences between cells in the substantia nigra and ventral tegmental area

Zhang

Shen

Jin

et al. 2007

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Neuronal oscillations have been suggested to play an important role in information processing in the brain. Using spectral analysis, we have recently shown that the repetitive burst-like firing in many dopamine (DA) neurons in the ventral tegmental area (VTA) can be described as a slow oscillation (SO) in firing rate. In this study, we examined whether DA neurons in the adjacent substantia nigra (SN) also display a SO. DA neurons were recorded extracellularly using the cells/track technique in chloral hydrate-anesthetized rats. Spectral analysis showed that firing patterns of SN DA neurons exhibited a SO similar to that observed in VTA DA neurons. The amplitude of the SO, however, was much reduced in the SN compared with that in the VTA and so was the number of DA neurons qualified as high-SO cells. In high-SO DA neurons, the amplitude of the SO was strongly correlated with the degree of bursting, and this correlation was observed in both the VTA and SN. In low-SO cells, however, the SO was more significantly correlated with the variability of firing than with firing rate and bursting. Since the generation of the SO depends on afferent inputs to DA neurons, a better understanding of its difference between the SN and VTA may provide important insights into the neural networks that control DA neurons in the two areas.

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Psychostimulants Induce Low-Frequency Oscillations in the Firing Activity of Dopamine Neurons

Cited by 60 publications

References 33 publications

Sensory effects of intravenous cocaine on dopamine and non-dopamine ventral tegmental area neurons

Sensory effects of intravenous cocaine on dopamine and non-dopamine ventral tegmental area neurons

Clozapine Blocks D-Amphetamine-Induced Excitation of Dopamine Neurons in the Ventral Tegmental Area

Oscillatory firing of dopamine neurons: Differences between cells in the substantia nigra and ventral tegmental area

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