Psychostimulants induce low-frequency oscillations in the firing activity of dopamine neurons
Abstract
The reinforcing properties of psychostimulants depend critically on their effects on dopamine (DA) neurons in the ventral tegmental area (VTA). Using in vivo single unit recording in rats and spectral analysis, this study presents evidence for a new, non-DA-mediated effect of psychostimulants on VTA DA neurons. Thus, as previously observed with D-amphetamine, all psychostimulants tested, including cocaine, methamphetamine, and methylphenidate, had two opposing effects on firing rate of DA neurons: a DA-mediated inhibition and a non-DA-mediated excitation. The latter effect was normally masked by the DA-mediated inhibition and was revealed when the inhibition was blocked by a DA antagonist. Using spectral analysis, this study further showed that during psychostimulant-induced excitation, DA cells exhibited not only an increase in firing rate and bursting but also a low-frequency rhythmic oscillation (0.5-1.5 Hz) in their firing activity. The oscillatory response was unique to psychostimulants since it was not observed with the GABA(A) agonist muscimol, which also increased DA cell firing, and not mimicked by the nonpsychostimulant DA agonist L-dopa. Results further suggest that the effect requires activation of adrenergic alpha1 receptors and depends on intact forebrain inputs to DA neurons. Further understanding of this novel effect may provide important insights into both the mechanism of action of psychostimulants and the neuronal circuitry that controls the activity of DA neurons in the brain.
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After administration of psychostimulants, including methylphenidate, the inhibitory effect prevails, leading to decreased responsiveness in dopaminergic neurons.
“After administration of psychostimulants (Bunney and Achajanian, 1976), including methylphenidate (Shi et al., 2004), the inhibitory effect prevails, leading to decreased responsiveness in dopaminergic neurons (Fig. 12B).”
From A positron emission tomography study of nigro-striatal dopaminergic mechanisms underlying attention: implications for ADHD and its treatment (2013) · cites this paper as Shi et al., 2004
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Backgrounddela Peña, I., Gevorkiana, R., & Shi, W.-X. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.07.044 · Cited by 116 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript Importantly, the effect of d-amphetamine is mimicked by all psychostimulants tested, but not by non-psychostimulant dopamine agonists including L-3,4-dihydroxyphenylalanine (Ldopa) (Shi et al., 2004).”
BackgroundInfluentialProlonged High Fat Diet Reduces Dopamine Reuptake without Altering DAT Gene Expression
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Cross-hemispheric dopamine projections have functional significance
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“During psychostimulant-induced excitation, VTA cells display slow, rhythmic oscillations (45).”
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“In contrast, activation of the presynaptic DA autoreceptors has been found to exert a strong inhibitory effect on the neuronal activity (Ruskin et al., 2001) and thereby result in the inhibition of the firing of DA neurons in the CNS (Bunney et al., 1973;Einhorn et al., 1988;Shi et al., 2000,2004).”
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“…Isoprotenerol iontophoresis Decreased firing rate (Aghajanian and Bunney, 1977; White and Wang, 1984) D2 VTA/SN NE Iontophoresis Decreased firing rate (Aghajanian and Bunney, 1977; White and Wang, 1984) NET VTA Nisoxetine i.v Increased slow oscillations and burst firing (Shi et al., 2004) Table 2.”
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“Alternatively, presynaptic dopamine autoreceptors may have prevented any further dopamine from being released from the presynaptic cell due to its inhibitory nature (Shi et al., 2004; Yang et al., 2006).”
BackgroundSlow Oscillatory Firing: A Major Firing Pattern of Dopamine Neurons in the Ventral Tegmental Area
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“Single-unit activities of VTA DA neurons were recorded extracellularly using techniques described previously (Shi et al. 2000, 2004).”
InfluentialCortical control of VTA function and influence on nicotine reward
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“Previous works in this laboratory and others have demonstrated that nearly 50 percentage of VTA DA neurons exhibits SO in basal condition and psychostimulants were found to alter SO [20,21].”
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“The effect is mimicked by the norepinephrine (NE) uptake blocker nisoxetine, but not by the indirect DA agonist L-dopa, and is eliminated by adrenergic 1 antagonists such as prazosin, suggesting that the effect is non-DA-mediated, involving activation of 1 receptors (Shi et al., 2000b, 2004).”
BackgroundMethodResultInfluentialOptical suppression of drug-evoked phasic dopamine release
McCutcheon, J. E., Cone, J. J., Sinon, C. G., Fortin, S. M., Kantak, P. A., Witten, I. B., Deisseroth, K. A., Stuber, G. D., & Roitman, M. F. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00114 · Cited by 25 · see citing works
“This finding is consistent with cocaine and raclopride stimulating burst firing in dopamine neurons (Shi et al., 2004) and somatic inhibition suppressing that activity.”
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“Single unit activities of VTA and SN DA neurons were recorded extracellularly using techniques similar to those described previously (Shi et al., 2000, 2004).”
BackgroundMethodLateral preoptic and ventral pallidal roles in locomotion and other movements
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“METH can decrease DA cell firing through tonic activation of D2 autoreceptors (Lin et al., 2016), whereas under D2 antagonism, this effect is reversed and METH will actually enhance the firing of DA neurons (Shi et al., 2004).”
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“This is in accordance with the pivotal role of a1-adrenergic receptor in the oscillatory firing of VTA DA neurons (Shi et al., 2004; Zhou et al., 2006).”
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“Instead, it is an effect of D-amphetamine unmasked when the D2-mediated inhibition is blocked by raclopride (Shi et al, 2000b, 2004).”
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“FFT-based phase analysis was performed using methods described previously (Gao et al., 2007; Shi et al., 2004).”
InfluentialComplexity of VTA DA neural activities in response to PFC transection in nicotine treated rats
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“PFC) [28,29].”
Porter‐Stransky, K. A., Wescott, S. A., Hershman, M., Badrinarayan, A., Weele, C. M. V., Lovic, V., & Aragona, B. J. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.08.028 · Cited by 11 · see citing works
“Finally, differential expression of midbrain autoreceptors [25] may be important for the regional specificity in unconditioned DA release evoked by cocaine since pretreatment with an autoreceptor blocker eliminates the core-shell differences in cocaine-evoked increases in DA concentration [1] and it is well establishe…”
BackgroundHeterogeneous extracellular dopamine regulation in the subregions of the olfactory tubercle
Park, J., Wakabayashi, K. T., Szalkowski, C. E., & Bhimani, R. V. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14069 · Cited by 11 · see citing works
Robinson, J. D., Howard, C. D., Pastuzyn, E. D., Byers, D. L., Keefe, K. A., & Garris, P. A. (2014) · Neurotoxicity Research · doi:10.1007/s12640-014-9459-y · Cited by 11 · see citing works
“This result is not entirely unexpected, as both pharmacologically evoked (Shi et al. 2000, 2004) and naturally occurring (Sombers et al. 2009; Owesson-White et al. 2012) DA transients are elicited by burst firing of DA neurons.”
BackgroundResultXu, D., Karain, B. D., Brantley, E. J., & Shi, W. (2011) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.110.177816 · Cited by 10 · see citing works
Chen, W., Volkow, N. D., Li, J., Pan, Y., & Du, C. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy057 · Cited by 10 · see citing works
Sannita, W. G., Carozzo, S., Orsini, P., Domenici, L., Porciatti, V., Fioretto, M., Garbarino, S., & Sartucci, F. (2009) · Vision Research · doi:10.1016/j.visres.2009.01.018 · Cited by 9 · see citing works
Rat globus pallidus neurons: Functional classification and effects of dopamine depletion
Karain, B. D., Xu, D., Bellone, J. A., Hartman, R. E., & Shi, W. (2014) · Synapse · doi:10.1002/syn.21783 · Cited by 8 · see citing works
“GP neurons were recorded extracellularly using techniques described previously (Gao et al., 2007; Shi et al., 2004; Shi, 2005).”
MethodMiceli, M. D., Omoloye, A., & Gronier, B. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110406 · Cited by 7 · see citing works
Liu, C., Wang, Y.-K., Jin, G.-Z., Shi, W., & Gao, M. (2018) · Scientific Reports · doi:10.1038/s41598-018-21592-7 · Cited by 6 · see citing works
Chen, T. Y., Zhang, D., Dragomir, A., Akay, Y. M., & Akay, M. (2011) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-011-0759-6 · Cited by 6 · see citing works
Pan, W. H. T., Hsieh, M., Wu, H.-H., & Lin, S. (2006) · Addiction Biology · doi:10.1111/j.1369-1600.2006.00044.x · Cited by 4 · see citing works
“Journal compilation © 2006 Society for the Study of Addiction Addiction Biology, 12, 51–58 56 Wynn H. T. Pan et al. DAT, then 5-HTT (Tanda et al. 1997; Fleckenstein, Gibb & Hanson 2000).”
BackgroundMethylphenidate modulates motor cortical dynamics and behaviorPreprint
Verhein, J. R., Vyas, S., & Shenoy, K. V. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.15.562405 · Cited by 3 · see citing works
Amphetamine Promotes Cortical Up State in Part Via Dopamine Receptors
Shen, G., & Shi, W. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.728729 · Cited by 2 · see citing works
Chen, T., Dragomir, A., Zhang, D., Akay, Y. M., & Akay, M. (2010) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2010.5626088 · Cited by 1 · see citing works
Cocaine and mefloquine-induced acute effects in ventral tegmental area dopamine and GABA neurons
Allison, D. W. (2009) · ScholarsArchive (Brigham Young University)
Krstenansky, J. L., Xu, D., Leitzke, R., Saldivar, A., Gevorkian, R. A., & Shi, W. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.08.015
“Amphetamine-like psychotomimetics also have an excitatory effect on DA neurons, which is in part mediated through adrenergic α1 receptors (Shi et al., 2000; Shi et al., 2004).”
Towards a Better Treatment of Parkinson's disease
Karain, B. D. (2014) · The Scholars Repository - LLU (Loma Linda University)
The effects of modafinil and atomoxetine on dopamine signaling in the striatal subregions of the rat
Bobák, M. (2015) · doi:10.30707/etd2015.bobak.m
“Under anesthesia, DAT-inhibiting psychomotor stimulants exert an inhibitory effect on DA neuron firing (Shi et al., 2000; Shi et al., 2004), yet an excitatory action in freely behaving rats (Koulchitsky et al., 2012).”
BackgroundResultInfluentialAdaptations in In Vivo Catecholamine Signaling in Models Of Stress and Addiction
Fox, M. E. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/me6d-mx57
Chalwadi, P. (2016) · doi:10.30707/etd2016.chalwadi.p
“Previous reports with other selective NET inhibitors, nisoxetine (Shi et al., 2000; Shi et al., 2004) and reboxetine (Linner et al., 2001), have also used i.v. administration at similar doses to demonstrate an activation of burst firing of midbrain DA neurons.”
BackgroundResultInfluentialPhasic dopamine release: its origin and function in reward seeking
Beyene, M. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/jt5q-0n02
- Authors
- Shi, W.-X., Pun, C.-L., & Zhou, Y.
- Affiliations
- Yale University (US)
- Corresponding author
- Shi, Wei-Xing
- Venue
- Neuropsychopharmacology
- Published
- 2004-07-14
- Volume
- 29
- Issue
- 12
- Pages
- 2160-2167
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- OpenAlex
- W2313888853
- Cited by
- 66
- References
- 38
- Citations by year
- 2023: 1 · 2022: 1 · 2021: 3 · 2019: 2 · 2018: 4 · 2017: 1 · 2016: 8 · 2015: 2 · 2014: 6 · 2013: 3 · 2012: 3
- FWCI
- 1.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- The Scholars Repository - LLU (Loma Linda University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- psychostimulants, dopaminergic neurons, ventral tegmental area, low-frequency oscillations, neuronal firing rate, cocaine, methamphetamine, methylphenidate, burst firing, muscimol, L-DOPA
- MeSH terms
- Action Potentials, Central Nervous System Stimulants, Animals, Dopamine, Drug Interactions, Functional Laterality, Male, Muscimol, Neurons, Periodicity, Spectrum Analysis, Dopamine Agents, Prosencephalon, Rats, Sprague-Dawley, Ventral Tegmental Area, GABA Agonists, Rats
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