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Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine
BACKGROUND: Among psychostimulants, the dopamine transporter ligands amphetamine and cocaine display the highest addictive potential; the adenosine receptor antagonist caffeine is most widely consumed but less addictive. Psychostimulant actions of amphetamine were correlated with its ability to orch...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8538898/ https://www.ncbi.nlm.nih.gov/pubmed/34278424 http://dx.doi.org/10.1093/ijnp/pyab049 |
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author | Valenti, Ornella Zambon, Alice Boehm, Stefan |
author_facet | Valenti, Ornella Zambon, Alice Boehm, Stefan |
author_sort | Valenti, Ornella |
collection | PubMed |
description | BACKGROUND: Among psychostimulants, the dopamine transporter ligands amphetamine and cocaine display the highest addictive potential; the adenosine receptor antagonist caffeine is most widely consumed but less addictive. Psychostimulant actions of amphetamine were correlated with its ability to orchestrate ventral tegmental dopamine neuron activity with contrasting shifts in firing after single vs repeated administration. Whether caffeine might impinge on dopamine neuron activity has remained elusive. METHODS: Population activity of ventral tegmental area dopamine neurons was determined by single-unit extracellular recordings and set in relation to mouse behavior in locomotion and conditioned place preference experiments, respectively. RESULTS: A single dose of caffeine reduced population activity as did amphetamine and the selective adenosine A2A antagonist KW-6002, but not the A1 antagonist DPCPX. Repeated administration of KW-6002 or amphetamine led to drug-conditioned place preference and to unaltered or even enhanced population activity. Recurrent injection of caffeine or DPCPX, in contrast, failed to cause conditioned place preference and persistently reduced population activity. Subsequent to repetitive drug administration, re-exposure to amphetamine or KW-6002, but not to caffeine or DPCPX, was able to reduce population activity. CONCLUSIONS: Behavioral sensitization to amphetamine is attributed to persistent activation of ventral tegmental area dopamine neurons via the ventral hippocampus. Accordingly, a switch from acute A2A receptor-mediated reduction of dopamine neuron population activity to enduring A1 receptor-mediated suppression is correlated with tolerance rather than sensitization in response to repeated caffeine intake. |
format | Online Article Text |
id | pubmed-8538898 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-85388982021-10-25 Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine Valenti, Ornella Zambon, Alice Boehm, Stefan Int J Neuropsychopharmacol Regular Research Articles BACKGROUND: Among psychostimulants, the dopamine transporter ligands amphetamine and cocaine display the highest addictive potential; the adenosine receptor antagonist caffeine is most widely consumed but less addictive. Psychostimulant actions of amphetamine were correlated with its ability to orchestrate ventral tegmental dopamine neuron activity with contrasting shifts in firing after single vs repeated administration. Whether caffeine might impinge on dopamine neuron activity has remained elusive. METHODS: Population activity of ventral tegmental area dopamine neurons was determined by single-unit extracellular recordings and set in relation to mouse behavior in locomotion and conditioned place preference experiments, respectively. RESULTS: A single dose of caffeine reduced population activity as did amphetamine and the selective adenosine A2A antagonist KW-6002, but not the A1 antagonist DPCPX. Repeated administration of KW-6002 or amphetamine led to drug-conditioned place preference and to unaltered or even enhanced population activity. Recurrent injection of caffeine or DPCPX, in contrast, failed to cause conditioned place preference and persistently reduced population activity. Subsequent to repetitive drug administration, re-exposure to amphetamine or KW-6002, but not to caffeine or DPCPX, was able to reduce population activity. CONCLUSIONS: Behavioral sensitization to amphetamine is attributed to persistent activation of ventral tegmental area dopamine neurons via the ventral hippocampus. Accordingly, a switch from acute A2A receptor-mediated reduction of dopamine neuron population activity to enduring A1 receptor-mediated suppression is correlated with tolerance rather than sensitization in response to repeated caffeine intake. Oxford University Press 2021-07-19 /pmc/articles/PMC8538898/ /pubmed/34278424 http://dx.doi.org/10.1093/ijnp/pyab049 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of CINP. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Regular Research Articles Valenti, Ornella Zambon, Alice Boehm, Stefan Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine |
title | Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine |
title_full | Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine |
title_fullStr | Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine |
title_full_unstemmed | Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine |
title_short | Orchestration of Dopamine Neuron Population Activity in the Ventral Tegmental Area by Caffeine: Comparison With Amphetamine |
title_sort | orchestration of dopamine neuron population activity in the ventral tegmental area by caffeine: comparison with amphetamine |
topic | Regular Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8538898/ https://www.ncbi.nlm.nih.gov/pubmed/34278424 http://dx.doi.org/10.1093/ijnp/pyab049 |
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