Cargando…

Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons

The ability of nitric oxide and acetylcholine to modulate the short-term plasticity of corticostriatal inputs was investigated using current-clamp recordings in BAC mouse brain slices. Glutamatergic responses were evoked by stimulation of corpus callosum in D1 and D2 dopamine receptor-expressing med...

Descripción completa

Detalles Bibliográficos
Autores principales: Blomeley, Craig P., Cains, Sarah, Bracci, Enrico
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4655244/
https://www.ncbi.nlm.nih.gov/pubmed/26635532
http://dx.doi.org/10.3389/fncel.2015.00453
_version_ 1782402157657456640
author Blomeley, Craig P.
Cains, Sarah
Bracci, Enrico
author_facet Blomeley, Craig P.
Cains, Sarah
Bracci, Enrico
author_sort Blomeley, Craig P.
collection PubMed
description The ability of nitric oxide and acetylcholine to modulate the short-term plasticity of corticostriatal inputs was investigated using current-clamp recordings in BAC mouse brain slices. Glutamatergic responses were evoked by stimulation of corpus callosum in D1 and D2 dopamine receptor-expressing medium spiny neurons (D1-MSNs and D2-MSN, respectively). Paired-pulse stimulation (50 ms intervals) evoked depressing or facilitating responses in subgroups of both D1-MSNs and D2 MSNs. In both neuronal types, glutamatergic responses of cells that displayed paired-pulse depression were not significantly affected by the nitric oxide donor S-nitroso-N-acetylpenicillamine (SNAP; 100 μM). Conversely, in D1-MSNs and D2-MSNs that displayed paired-pulse facilitation, SNAP did not affect the first evoked response, but significantly reduced the amplitude of the second evoked EPSP, converting paired-pulse facilitation into paired-pulse depression. SNAP also strongly excited cholinergic interneurons and increased their cortical glutamatergic responses acting through a presynaptic mechanism. The effects of SNAP on glutamatergic response of D1-MSNs and D2-MSN were mediated by acetylcholine. The broad-spectrum muscarinic receptor antagonist atropine (25 μM) did not affect paired-pulse ratios and did not prevent the effects of SNAP. Conversely, the broad-spectrum nicotinic receptor antagonist tubocurarine (10 μM) fully mimicked and occluded the effects of SNAP. We concluded that phasic acetylcholine release mediates feedforward facilitation in MSNs through activation of nicotinic receptors on glutamatergic terminals and that nitric oxide, while increasing cholinergic interneurons’ firing, functionally impairs their ability to modulate glutamatergic inputs of MSNs. These results show that nitrergic and cholinergic transmission control the short-term plasticity of glutamatergic inputs in the striatum and reveal a novel cellular mechanism underlying paired-pulse facilitation in this area.
format Online
Article
Text
id pubmed-4655244
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-46552442015-12-03 Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons Blomeley, Craig P. Cains, Sarah Bracci, Enrico Front Cell Neurosci Neuroscience The ability of nitric oxide and acetylcholine to modulate the short-term plasticity of corticostriatal inputs was investigated using current-clamp recordings in BAC mouse brain slices. Glutamatergic responses were evoked by stimulation of corpus callosum in D1 and D2 dopamine receptor-expressing medium spiny neurons (D1-MSNs and D2-MSN, respectively). Paired-pulse stimulation (50 ms intervals) evoked depressing or facilitating responses in subgroups of both D1-MSNs and D2 MSNs. In both neuronal types, glutamatergic responses of cells that displayed paired-pulse depression were not significantly affected by the nitric oxide donor S-nitroso-N-acetylpenicillamine (SNAP; 100 μM). Conversely, in D1-MSNs and D2-MSNs that displayed paired-pulse facilitation, SNAP did not affect the first evoked response, but significantly reduced the amplitude of the second evoked EPSP, converting paired-pulse facilitation into paired-pulse depression. SNAP also strongly excited cholinergic interneurons and increased their cortical glutamatergic responses acting through a presynaptic mechanism. The effects of SNAP on glutamatergic response of D1-MSNs and D2-MSN were mediated by acetylcholine. The broad-spectrum muscarinic receptor antagonist atropine (25 μM) did not affect paired-pulse ratios and did not prevent the effects of SNAP. Conversely, the broad-spectrum nicotinic receptor antagonist tubocurarine (10 μM) fully mimicked and occluded the effects of SNAP. We concluded that phasic acetylcholine release mediates feedforward facilitation in MSNs through activation of nicotinic receptors on glutamatergic terminals and that nitric oxide, while increasing cholinergic interneurons’ firing, functionally impairs their ability to modulate glutamatergic inputs of MSNs. These results show that nitrergic and cholinergic transmission control the short-term plasticity of glutamatergic inputs in the striatum and reveal a novel cellular mechanism underlying paired-pulse facilitation in this area. Frontiers Media S.A. 2015-11-23 /pmc/articles/PMC4655244/ /pubmed/26635532 http://dx.doi.org/10.3389/fncel.2015.00453 Text en Copyright © 2015 Blomeley, Cains and Bracci. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Blomeley, Craig P.
Cains, Sarah
Bracci, Enrico
Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons
title Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons
title_full Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons
title_fullStr Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons
title_full_unstemmed Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons
title_short Dual Nitrergic/Cholinergic Control of Short-Term Plasticity of Corticostriatal Inputs to Striatal Projection Neurons
title_sort dual nitrergic/cholinergic control of short-term plasticity of corticostriatal inputs to striatal projection neurons
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4655244/
https://www.ncbi.nlm.nih.gov/pubmed/26635532
http://dx.doi.org/10.3389/fncel.2015.00453
work_keys_str_mv AT blomeleycraigp dualnitrergiccholinergiccontrolofshorttermplasticityofcorticostriatalinputstostriatalprojectionneurons
AT cainssarah dualnitrergiccholinergiccontrolofshorttermplasticityofcorticostriatalinputstostriatalprojectionneurons
AT braccienrico dualnitrergiccholinergiccontrolofshorttermplasticityofcorticostriatalinputstostriatalprojectionneurons