Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents

The firing of striatal projection neurons (SPNs) exhibits afterhyperpolarizing potentials (AHPs) that determine discharge frequency. They are in part generated by Ca2+-activated K+-currents involving BK and SK components. It has previously been shown that suprathreshold corticostriatal responses are...

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Main Authors: Mario Alberto Arias-García, Dagoberto eTapia, Edén eFlores-Barrera, Jesús Esteban Pérez-Ortega, Jose eBargas, Elvira eGalarraga
Format: Article
Language:English
Published: Frontiers Media S.A. 2013-10-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnsys.2013.00063/full
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author Mario Alberto Arias-García
Dagoberto eTapia
Edén eFlores-Barrera
Jesús Esteban Pérez-Ortega
Jose eBargas
Elvira eGalarraga
author_facet Mario Alberto Arias-García
Dagoberto eTapia
Edén eFlores-Barrera
Jesús Esteban Pérez-Ortega
Jose eBargas
Elvira eGalarraga
author_sort Mario Alberto Arias-García
collection DOAJ
description The firing of striatal projection neurons (SPNs) exhibits afterhyperpolarizing potentials (AHPs) that determine discharge frequency. They are in part generated by Ca2+-activated K+-currents involving BK and SK components. It has previously been shown that suprathreshold corticostriatal responses are more prolonged and evoke more action potentials in direct pathway SPNs (dSPNs) than in indirect pathway SPNs (iSPNs). In contrast, iSPNs generate dendritic autoregenerative responses. Using whole cell recordings in brain slices, we asked whether the participation of Ca2+-activated K+-currents plays a role in these responses. Secondly, we asked if these currents may explain some differences in synaptic integration between dSPNs and iSPNs. Neurons obtained from BAC D1 and D2 GFP mice were recorded. We used charybdotoxin and apamin to block BK and SK channels, respectively. Both antagonists increased the depolarization and delayed the repolarization of suprathreshold corticostriatal responses in both neuron classes. We also used NS 1619 and NS 309 (CyPPA), to enhance BK and SK channels, respectively. Current enhancers hyperpolarized and accelerated the repolarization of corticostriatal responses in both neuron classes. These drugs made evident that the contribution of Ca2+-activated K+-currents was different in dSPNs as compared to iSPNs: in dSPNs their activation was slower as though calcium took a diffusion delay to activate them. In contrast, their activation was fast and then sustained in iSPNs as though calcium flux activates them at the moment of entry. The blockade of Ca2+-activated K+-currents made iSPNs to look as dSPNs. Conversely, their enhancement made dSPNs to look as iSPNs. It is concluded that Ca2+-activated K+-currents are a main intrinsic determinant causing the differences in synaptic integration between corticostriatal polysynaptic responses between dSPNs and iSPNs.
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spelling doaj.art-4cc1955a5a3d4db7a650f36b2791a5322022-12-21T18:26:41ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372013-10-01710.3389/fnsys.2013.0006364944Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currentsMario Alberto Arias-García0Dagoberto eTapia1Edén eFlores-Barrera2Jesús Esteban Pérez-Ortega3Jose eBargas4Elvira eGalarraga5Universidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoUniversidad Nacional Autónoma de MéxicoThe firing of striatal projection neurons (SPNs) exhibits afterhyperpolarizing potentials (AHPs) that determine discharge frequency. They are in part generated by Ca2+-activated K+-currents involving BK and SK components. It has previously been shown that suprathreshold corticostriatal responses are more prolonged and evoke more action potentials in direct pathway SPNs (dSPNs) than in indirect pathway SPNs (iSPNs). In contrast, iSPNs generate dendritic autoregenerative responses. Using whole cell recordings in brain slices, we asked whether the participation of Ca2+-activated K+-currents plays a role in these responses. Secondly, we asked if these currents may explain some differences in synaptic integration between dSPNs and iSPNs. Neurons obtained from BAC D1 and D2 GFP mice were recorded. We used charybdotoxin and apamin to block BK and SK channels, respectively. Both antagonists increased the depolarization and delayed the repolarization of suprathreshold corticostriatal responses in both neuron classes. We also used NS 1619 and NS 309 (CyPPA), to enhance BK and SK channels, respectively. Current enhancers hyperpolarized and accelerated the repolarization of corticostriatal responses in both neuron classes. These drugs made evident that the contribution of Ca2+-activated K+-currents was different in dSPNs as compared to iSPNs: in dSPNs their activation was slower as though calcium took a diffusion delay to activate them. In contrast, their activation was fast and then sustained in iSPNs as though calcium flux activates them at the moment of entry. The blockade of Ca2+-activated K+-currents made iSPNs to look as dSPNs. Conversely, their enhancement made dSPNs to look as iSPNs. It is concluded that Ca2+-activated K+-currents are a main intrinsic determinant causing the differences in synaptic integration between corticostriatal polysynaptic responses between dSPNs and iSPNs.http://journal.frontiersin.org/Journal/10.3389/fnsys.2013.00063/fullStriatumSK channelsBK channelsSynaptic integrationcorticostriatal pathwayMedium spiny neurons
spellingShingle Mario Alberto Arias-García
Dagoberto eTapia
Edén eFlores-Barrera
Jesús Esteban Pérez-Ortega
Jose eBargas
Elvira eGalarraga
Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents
Frontiers in Systems Neuroscience
Striatum
SK channels
BK channels
Synaptic integration
corticostriatal pathway
Medium spiny neurons
title Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents
title_full Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents
title_fullStr Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents
title_full_unstemmed Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents
title_short Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents
title_sort duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents
topic Striatum
SK channels
BK channels
Synaptic integration
corticostriatal pathway
Medium spiny neurons
url http://journal.frontiersin.org/Journal/10.3389/fnsys.2013.00063/full
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