Global actions of nicotine on the striatal microcircuit

The question to solve in the present work is: what is the predominant action induced by the activation of cholinergic-nicotinic receptors (nAChrs) in the striatal network given that nAChrs are expressed by several elements of the circuit: cortical terminals, dopamine terminals, and various striatal...

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Main Authors: Victor E Plata, Mariana eDuhne, Jesús Esteban Pérez-Ortega, Ricardo eHernandez-Martinez, Pavel Ernesto Rueda Orozco, Elvira eGalarraga, Rene eDrucker-Colin, Jose eBargas
Format: Article
Language:English
Published: Frontiers Media S.A. 2013-11-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnsys.2013.00078/full
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author Victor E Plata
Mariana eDuhne
Jesús Esteban Pérez-Ortega
Ricardo eHernandez-Martinez
Pavel Ernesto Rueda Orozco
Elvira eGalarraga
Rene eDrucker-Colin
Jose eBargas
author_facet Victor E Plata
Mariana eDuhne
Jesús Esteban Pérez-Ortega
Ricardo eHernandez-Martinez
Pavel Ernesto Rueda Orozco
Elvira eGalarraga
Rene eDrucker-Colin
Jose eBargas
author_sort Victor E Plata
collection DOAJ
description The question to solve in the present work is: what is the predominant action induced by the activation of cholinergic-nicotinic receptors (nAChrs) in the striatal network given that nAChrs are expressed by several elements of the circuit: cortical terminals, dopamine terminals, and various striatal GABAergic interneurons. To answer this question some type of multicellular recording has to be used without losing single cell resolution. Here, we used calcium imaging and nicotine. It is known that in the presence of low micromolar N-Methyl-D-aspartate (NMDA), the striatal microcircuit exhibits neuronal activity consisting in the spontaneous synchronization of different neuron pools that interchange their activity following determined sequences. The striatal circuit also exhibits profuse spontaneous activity in pathological states (without NMDA) such as dopamine depletion. However, in this case, most pathological activity is mostly generated by the same neuron pool. Here, we show that both types of activity are inhibited during the application of nicotine. Nicotine actions were blocked by mecamylamine, a non specific antagonist of nAChrs. Interestingly, inhibitory actions of nicotine were also blocked by the GABAA-receptor antagonist bicuculline, in which case, the actions of nicotine on the circuit became excitatory and facilitated neuronal synchronization. We conclude that the predominant action of nicotine in the striatal microcircuit is indirect, via the activation of networks of inhibitory interneurons. This action inhibits striatal pathological activity in early Parkinsonian animals almost as potently as L-DOPA.
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spelling doaj.art-9b51c571a9994f90b294052efe744d2a2022-12-21T20:31:06ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372013-11-01710.3389/fnsys.2013.0007864926Global actions of nicotine on the striatal microcircuitVictor E Plata0Mariana eDuhne1Jesús Esteban Pérez-Ortega2Ricardo eHernandez-Martinez3Pavel Ernesto Rueda Orozco4Elvira eGalarraga5Rene eDrucker-Colin6Jose eBargas7Universidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de México (University, Governmental)Universidad Nacional Autónoma de MéxicoThe question to solve in the present work is: what is the predominant action induced by the activation of cholinergic-nicotinic receptors (nAChrs) in the striatal network given that nAChrs are expressed by several elements of the circuit: cortical terminals, dopamine terminals, and various striatal GABAergic interneurons. To answer this question some type of multicellular recording has to be used without losing single cell resolution. Here, we used calcium imaging and nicotine. It is known that in the presence of low micromolar N-Methyl-D-aspartate (NMDA), the striatal microcircuit exhibits neuronal activity consisting in the spontaneous synchronization of different neuron pools that interchange their activity following determined sequences. The striatal circuit also exhibits profuse spontaneous activity in pathological states (without NMDA) such as dopamine depletion. However, in this case, most pathological activity is mostly generated by the same neuron pool. Here, we show that both types of activity are inhibited during the application of nicotine. Nicotine actions were blocked by mecamylamine, a non specific antagonist of nAChrs. Interestingly, inhibitory actions of nicotine were also blocked by the GABAA-receptor antagonist bicuculline, in which case, the actions of nicotine on the circuit became excitatory and facilitated neuronal synchronization. We conclude that the predominant action of nicotine in the striatal microcircuit is indirect, via the activation of networks of inhibitory interneurons. This action inhibits striatal pathological activity in early Parkinsonian animals almost as potently as L-DOPA.http://journal.frontiersin.org/Journal/10.3389/fnsys.2013.00078/fullBasal GangliaNicotinenicotinic receptorsGABAergic interneuronsparkinson´s diseasestriatal microcircuit
spellingShingle Victor E Plata
Mariana eDuhne
Jesús Esteban Pérez-Ortega
Ricardo eHernandez-Martinez
Pavel Ernesto Rueda Orozco
Elvira eGalarraga
Rene eDrucker-Colin
Jose eBargas
Global actions of nicotine on the striatal microcircuit
Frontiers in Systems Neuroscience
Basal Ganglia
Nicotine
nicotinic receptors
GABAergic interneurons
parkinson´s disease
striatal microcircuit
title Global actions of nicotine on the striatal microcircuit
title_full Global actions of nicotine on the striatal microcircuit
title_fullStr Global actions of nicotine on the striatal microcircuit
title_full_unstemmed Global actions of nicotine on the striatal microcircuit
title_short Global actions of nicotine on the striatal microcircuit
title_sort global actions of nicotine on the striatal microcircuit
topic Basal Ganglia
Nicotine
nicotinic receptors
GABAergic interneurons
parkinson´s disease
striatal microcircuit
url http://journal.frontiersin.org/Journal/10.3389/fnsys.2013.00078/full
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