Literature DB >> 28827326

Cell-type-specific inhibition of the dendritic plateau potential in striatal spiny projection neurons.

Kai Du1,2, Yu-Wei Wu3,4, Robert Lindroos1,2, Yu Liu3,4, Balázs Rózsa5, Gergely Katona6, Jun B Ding7,4, Jeanette Hellgren Kotaleski8,2,9.   

Abstract

Striatal spiny projection neurons (SPNs) receive convergent excitatory synaptic inputs from the cortex and thalamus. Activation of spatially clustered and temporally synchronized excitatory inputs at the distal dendrites could trigger plateau potentials in SPNs. Such supralinear synaptic integration is crucial for dendritic computation. However, how plateau potentials interact with subsequent excitatory and inhibitory synaptic inputs remains unknown. By combining computational simulation, two-photon imaging, optogenetics, and dual-color uncaging of glutamate and GABA, we demonstrate that plateau potentials can broaden the spatiotemporal window for integrating excitatory inputs and promote spiking. The temporal window of spiking can be delicately controlled by GABAergic inhibition in a cell-type-specific manner. This subtle inhibitory control of plateau potential depends on the location and kinetics of the GABAergic inputs and is achieved by the balance between relief and reestablishment of NMDA receptor Mg2+ block. These findings represent a mechanism for controlling spatiotemporal synaptic integration in SPNs.

Entities:  

Keywords:  dendritic computation; inhibition; plateau potential; striatum; synaptic integration

Mesh:

Substances:

Year:  2017        PMID: 28827326      PMCID: PMC5594658          DOI: 10.1073/pnas.1704893114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  56 in total

1.  Dependence of GABAergic synaptic areas on the interneuron type and target size.

Authors:  Y Kubota; Y Kawaguchi
Journal:  J Neurosci       Date:  2000-01-01       Impact factor: 6.167

2.  Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell.

Authors:  Panayiota Poirazi; Terrence Brannon; Bartlett W Mel
Journal:  Neuron       Date:  2003-03-27       Impact factor: 17.173

3.  Regulation of neuronal input transformations by tunable dendritic inhibition.

Authors:  Matthew Lovett-Barron; Gergely F Turi; Patrick Kaifosh; Peter H Lee; Frédéric Bolze; Xiao-Hua Sun; Jean-François Nicoud; Boris V Zemelman; Scott M Sternson; Attila Losonczy
Journal:  Nat Neurosci       Date:  2012-01-15       Impact factor: 24.884

4.  Dendritic spikes induce ripples in parvalbumin interneurons during hippocampal sharp waves.

Authors:  Balázs Chiovini; Gergely F Turi; Gergely Katona; Attila Kaszás; Dénes Pálfi; Pál Maák; Gergely Szalay; Mátyás Forián Szabó; Gábor Szabó; Zoltán Szadai; Szabolcs Káli; Balázs Rózsa
Journal:  Neuron       Date:  2014-05-21       Impact factor: 17.173

5.  Distinct roles of GABAergic interneurons in the regulation of striatal output pathways.

Authors:  Aryn H Gittis; Alexandra B Nelson; Myo T Thwin; Jorge J Palop; Anatol C Kreitzer
Journal:  J Neurosci       Date:  2010-02-10       Impact factor: 6.167

6.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons.

Authors:  C J Wilson; Y Kawaguchi
Journal:  J Neurosci       Date:  1996-04-01       Impact factor: 6.167

7.  Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo.

Authors:  E A Stern; A E Kincaid; C J Wilson
Journal:  J Neurophysiol       Date:  1997-04       Impact factor: 2.714

8.  Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease.

Authors:  Stefano Taverna; Ema Ilijic; D James Surmeier
Journal:  J Neurosci       Date:  2008-05-21       Impact factor: 6.167

9.  The effects of NMDA subunit composition on calcium influx and spike timing-dependent plasticity in striatal medium spiny neurons.

Authors:  Rebekah C Evans; Teresa Morera-Herreras; Yihui Cui; Kai Du; Tom Sheehan; Jeanette Hellgren Kotaleski; Laurent Venance; Kim T Blackwell
Journal:  PLoS Comput Biol       Date:  2012-04-19       Impact factor: 4.475

10.  Glutamate-bound NMDARs arising from in vivo-like network activity extend spatio-temporal integration in a L5 cortical pyramidal cell model.

Authors:  Matteo Farinella; Daniel T Ruedt; Padraig Gleeson; Frederic Lanore; R Angus Silver
Journal:  PLoS Comput Biol       Date:  2014-04-24       Impact factor: 4.475

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  21 in total

Review 1.  Dopaminergic modulation of striatal function and Parkinson's disease.

Authors:  Shenyu Zhai; Weixing Shen; Steven M Graves; D James Surmeier
Journal:  J Neural Transm (Vienna)       Date:  2019-04-01       Impact factor: 3.575

2.  Connectivity and Dynamics Underlying Synaptic Control of the Subthalamic Nucleus.

Authors:  Leon Amadeus Steiner; Federico J Barreda Tomás; Henrike Planert; Henrik Alle; Imre Vida; Jörg R P Geiger
Journal:  J Neurosci       Date:  2019-01-30       Impact factor: 6.167

3.  Hippocampal-Evoked Feedforward Inhibition in the Nucleus Accumbens.

Authors:  Samantha L Scudder; Corey Baimel; Emma E Macdonald; Adam G Carter
Journal:  J Neurosci       Date:  2018-09-05       Impact factor: 6.167

Review 4.  From membrane receptors to protein synthesis and actin cytoskeleton: Mechanisms underlying long lasting forms of synaptic plasticity.

Authors:  Joanna Jędrzejewska-Szmek; Kim T Blackwell
Journal:  Semin Cell Dev Biol       Date:  2019-01-12       Impact factor: 7.727

5.  Transient Response of Basal Ganglia Network in Healthy and Low-Dopamine State.

Authors:  Kingshuk Chakravarty; Sangheeta Roy; Aniruddha Sinha; Atsushi Nambu; Satomi Chiken; Jeanette Hellgren Kotaleski; Arvind Kumar
Journal:  eNeuro       Date:  2022-03-18

6.  Noise-induced properties of active dendrites.

Authors:  Carl van Vreeswijk; Farzada Farkhooi
Journal:  Proc Natl Acad Sci U S A       Date:  2021-08-24       Impact factor: 11.205

7.  Motor learning selectively strengthens cortical and striatal synapses of motor engram neurons.

Authors:  Fuu-Jiun Hwang; Richard H Roth; Yu-Wei Wu; Yue Sun; Destany K Kwon; Yu Liu; Jun B Ding
Journal:  Neuron       Date:  2022-07-08       Impact factor: 18.688

Review 8.  Striatal synaptic adaptations in Parkinson's disease.

Authors:  Weixing Shen; Shenyu Zhai; D James Surmeier
Journal:  Neurobiol Dis       Date:  2022-03-08       Impact factor: 7.046

9.  Local glutamate-mediated dendritic plateau potentials change the state of the cortical pyramidal neuron.

Authors:  Peng P Gao; Joseph W Graham; Wen-Liang Zhou; Jinyoung Jang; Sergio Angulo; Salvador Dura-Bernal; Michael Hines; William W Lytton; Srdjan D Antic
Journal:  J Neurophysiol       Date:  2020-10-21       Impact factor: 2.714

10.  Dopamine Oppositely Modulates State Transitions in Striosome and Matrix Direct Pathway Striatal Spiny Neurons.

Authors:  Eric M Prager; Daniel B Dorman; Zachary B Hobel; Jeffrey M Malgady; Kim T Blackwell; Joshua L Plotkin
Journal:  Neuron       Date:  2020-10-19       Impact factor: 17.173

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