Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release

Abstract Neuronal networks cause changes in behaviorally important information processing through the vesicular release of neurotransmitters governed by the rate and timing of action potentials (APs). Herein, we provide evidence that dopamine (DA), nonquantally released from the cytoplasm, may exert...

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Autores principales:	Viktor Román, Rita Kedves, Kristóf Kelemen, Zsolt Némethy, Beáta Sperlágh, Balázs Lendvai, E. Sylvester Vizi
Formato:	article
Lenguaje:	EN
Publicado:	Wiley 2021
Materias:	cytoplasmic release dopamine nonquantal social behavior transporter Physiology QP1-981
Acceso en línea:	https://doaj.org/article/e408a6cb2205436dbb66a18baeb6f2a5
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spelling	oai:doaj.org-article:e408a6cb2205436dbb66a18baeb6f2a52021-11-15T09:54:41ZContribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release2051-817X10.14814/phy2.15088https://doaj.org/article/e408a6cb2205436dbb66a18baeb6f2a52021-11-01T00:00:00Zhttps://doi.org/10.14814/phy2.15088https://doaj.org/toc/2051-817XAbstract Neuronal networks cause changes in behaviorally important information processing through the vesicular release of neurotransmitters governed by the rate and timing of action potentials (APs). Herein, we provide evidence that dopamine (DA), nonquantally released from the cytoplasm, may exert similar effects in vivo. In mouse slice preparations, (+/−)‐3,4‐methylenedioxy‐methamphetamine (MDMA, or ecstasy) and β‐phenylethylamine (β‐PEA)‐induced DA release in the striatum and nucleus accumbens (NAc), two regions of the brain involved in reward‐driven and social behavior and inhibited the axonal stimulation‐induced release of tritiated acetylcholine ([3H]ACh) in the striatum. The DA transporter (DAT) inhibitor (GBR‐12909) prevented MDMA and β‐PEA from causing DA release. GBR‐12909 could also restore some of the stimulated acetylcholine release reduced by MDMA or β‐PEA in the striatum confirming the fundamental role of DAT. In addition, hypothermia could prevent the β‐PEA‐induced release in the striatum and in the NAc. Sulpiride, a D2 receptor antagonist, also prevented the inhibitory effects of MDMA or β‐PEA on stimulated ACh release, suggesting they act indirectly via binding of DA. Reflecting the neurochemical interactions in brain slices at higher system level, MDMA altered the social behavior of rats by preferentially enhancing passive social behavior. Similar to the in vitro effects, GBR‐12909 treatment reversed specific elements of the MDMA‐induced changes in behavior, such as passive social behavior, while left others including social play unchanged. The changes in behavior by the high level of extracellular DA–– a significant amount originating from cytoplasmic release––suggest that in addition to digital computation through synapses, the brain also uses analog communication, such as DA signaling, to mediate some elements of complex behaviors, but in a much longer time scale.Viktor RománRita KedvesKristóf KelemenZsolt NémethyBeáta SperlághBalázs LendvaiE. Sylvester ViziWileyarticlecytoplasmic releasedopaminenonquantalsocial behaviortransporterPhysiologyQP1-981ENPhysiological Reports, Vol 9, Iss 21, Pp n/a-n/a (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	cytoplasmic release dopamine nonquantal social behavior transporter Physiology QP1-981
spellingShingle	cytoplasmic release dopamine nonquantal social behavior transporter Physiology QP1-981 Viktor Román Rita Kedves Kristóf Kelemen Zsolt Némethy Beáta Sperlágh Balázs Lendvai E. Sylvester Vizi Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release
description	Abstract Neuronal networks cause changes in behaviorally important information processing through the vesicular release of neurotransmitters governed by the rate and timing of action potentials (APs). Herein, we provide evidence that dopamine (DA), nonquantally released from the cytoplasm, may exert similar effects in vivo. In mouse slice preparations, (+/−)‐3,4‐methylenedioxy‐methamphetamine (MDMA, or ecstasy) and β‐phenylethylamine (β‐PEA)‐induced DA release in the striatum and nucleus accumbens (NAc), two regions of the brain involved in reward‐driven and social behavior and inhibited the axonal stimulation‐induced release of tritiated acetylcholine ([3H]ACh) in the striatum. The DA transporter (DAT) inhibitor (GBR‐12909) prevented MDMA and β‐PEA from causing DA release. GBR‐12909 could also restore some of the stimulated acetylcholine release reduced by MDMA or β‐PEA in the striatum confirming the fundamental role of DAT. In addition, hypothermia could prevent the β‐PEA‐induced release in the striatum and in the NAc. Sulpiride, a D2 receptor antagonist, also prevented the inhibitory effects of MDMA or β‐PEA on stimulated ACh release, suggesting they act indirectly via binding of DA. Reflecting the neurochemical interactions in brain slices at higher system level, MDMA altered the social behavior of rats by preferentially enhancing passive social behavior. Similar to the in vitro effects, GBR‐12909 treatment reversed specific elements of the MDMA‐induced changes in behavior, such as passive social behavior, while left others including social play unchanged. The changes in behavior by the high level of extracellular DA–– a significant amount originating from cytoplasmic release––suggest that in addition to digital computation through synapses, the brain also uses analog communication, such as DA signaling, to mediate some elements of complex behaviors, but in a much longer time scale.
format	article
author	Viktor Román Rita Kedves Kristóf Kelemen Zsolt Némethy Beáta Sperlágh Balázs Lendvai E. Sylvester Vizi
author_facet	Viktor Román Rita Kedves Kristóf Kelemen Zsolt Némethy Beáta Sperlágh Balázs Lendvai E. Sylvester Vizi
author_sort	Viktor Román
title	Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release
title_short	Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release
title_full	Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release
title_fullStr	Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release
title_full_unstemmed	Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release
title_sort	contribution of analog signaling to neurotransmitter interactions and behavior: role of transporter‐mediated nonquantal dopamine release
publisher	Wiley
publishDate	2021
url	https://doaj.org/article/e408a6cb2205436dbb66a18baeb6f2a5
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_version_	1718428466748063744

Contribution of analog signaling to neurotransmitter interactions and behavior: Role of transporter‐mediated nonquantal dopamine release

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