Literature DB >> 20080772

Distinct nonuniform cable properties optimize rapid and efficient activation of fast-spiking GABAergic interneurons.

Anja Nörenberg1, Hua Hu, Imre Vida, Marlene Bartos, Peter Jonas.   

Abstract

Fast-spiking, parvalbumin-expressing basket cells (BCs) play a key role in feedforward and feedback inhibition in the hippocampus. However, the dendritic mechanisms underlying rapid interneuron recruitment have remained unclear. To quantitatively address this question, we developed detailed passive cable models of BCs in the dentate gyrus based on dual somatic or somatodendritic recordings and complete morphologic reconstructions. Both specific membrane capacitance and axial resistivity were comparable to those of pyramidal neurons, but the average somatodendritic specific membrane resistance (R(m)) was substantially lower in BCs. Furthermore, R(m) was markedly nonuniform, being lowest in soma and proximal dendrites, intermediate in distal dendrites, and highest in the axon. Thus, the somatodendritic gradient of R(m) was the reverse of that in pyramidal neurons. Further computational analysis revealed that these unique cable properties accelerate the time course of synaptic potentials at the soma in response to fast inputs, while boosting the efficacy of slow distal inputs. These properties will facilitate both rapid phasic and efficient tonic activation of BCs in hippocampal microcircuits.

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Year:  2009        PMID: 20080772      PMCID: PMC2818894          DOI: 10.1073/pnas.0910716107

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


  35 in total

Review 1.  Interneurons unbound.

Authors:  C J McBain; A Fisahn
Journal:  Nat Rev Neurosci       Date:  2001-01       Impact factor: 34.870

2.  Passive normalization of synaptic integration influenced by dendritic architecture.

Authors:  D B Jaffe; N T Carnevale
Journal:  J Neurophysiol       Date:  1999-12       Impact factor: 2.714

3.  Direct measurement of specific membrane capacitance in neurons.

Authors:  L J Gentet; G J Stuart; J D Clements
Journal:  Biophys J       Date:  2000-07       Impact factor: 4.033

Review 4.  Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing.

Authors:  B Rudy; C J McBain
Journal:  Trends Neurosci       Date:  2001-09       Impact factor: 13.837

Review 5.  Theta oscillations in the hippocampus.

Authors:  György Buzsáki
Journal:  Neuron       Date:  2002-01-31       Impact factor: 17.173

6.  Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition.

Authors:  F Pouille; M Scanziani
Journal:  Science       Date:  2001-08-10       Impact factor: 47.728

7.  Active dendrites and spike propagation in multi-compartment models of oriens-lacunosum/moleculare hippocampal interneurons.

Authors:  F Saraga; C P Wu; L Zhang; F K Skinner
Journal:  J Physiol       Date:  2003-08-15       Impact factor: 5.182

8.  Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse.

Authors:  Iancu Bucurenciu; Akos Kulik; Beat Schwaller; Michael Frotscher; Peter Jonas
Journal:  Neuron       Date:  2008-02-28       Impact factor: 17.173

9.  Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons.

Authors:  Hua Hu; Marco Martina; Peter Jonas
Journal:  Science       Date:  2009-12-03       Impact factor: 47.728

10.  Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings.

Authors:  A Roth; M Häusser
Journal:  J Physiol       Date:  2001-09-01       Impact factor: 5.182

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  52 in total

1.  Fast activation of feedforward inhibitory neurons from thalamic input and its relevance to the regulation of spike sequences in the barrel cortex.

Authors:  Fumitaka Kimura; Chiaki Itami; Koji Ikezoe; Hiroshi Tamura; Ichiro Fujita; Yuchio Yanagawa; Kunihiko Obata; Minoru Ohshima
Journal:  J Physiol       Date:  2010-06-07       Impact factor: 5.182

2.  Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice.

Authors:  Csaba Varga; Peyman Golshani; Ivan Soltesz
Journal:  Proc Natl Acad Sci U S A       Date:  2012-09-10       Impact factor: 11.205

3.  Enhanced high-frequency membrane potential fluctuations control spike output in striatal fast-spiking interneurones in vivo.

Authors:  Jan M Schulz; Toni L Pitcher; Shakuntala Savanthrapadian; Jeffery R Wickens; Manfred J Oswald; John N J Reynolds
Journal:  J Physiol       Date:  2011-07-11       Impact factor: 5.182

4.  Functional properties of GABA synaptic inputs onto GABA neurons in monkey prefrontal cortex.

Authors:  Diana C Rotaru; Cameron Olezene; Takeaki Miyamae; Nadezhda V Povysheva; Aleksey V Zaitsev; David A Lewis; Guillermo Gonzalez-Burgos
Journal:  J Neurophysiol       Date:  2014-12-24       Impact factor: 2.714

5.  Regulation of AMPA and NMDA receptor-mediated EPSPs in dendritic trees of thalamocortical cells.

Authors:  Francis Lajeunesse; Helmut Kröger; Igor Timofeev
Journal:  J Neurophysiol       Date:  2012-10-24       Impact factor: 2.714

6.  Developmental pruning of excitatory synaptic inputs to parvalbumin interneurons in monkey prefrontal cortex.

Authors:  Daniel W Chung; Zachary P Wills; Kenneth N Fish; David A Lewis
Journal:  Proc Natl Acad Sci U S A       Date:  2017-01-10       Impact factor: 11.205

Review 7.  Highly energized inhibitory interneurons are a central element for information processing in cortical networks.

Authors:  Oliver Kann; Ismini E Papageorgiou; Andreas Draguhn
Journal:  J Cereb Blood Flow Metab       Date:  2014-06-04       Impact factor: 6.200

Review 8.  GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits.

Authors:  Robin Tremblay; Soohyun Lee; Bernardo Rudy
Journal:  Neuron       Date:  2016-07-20       Impact factor: 17.173

Review 9.  Normal and epilepsy-associated pathologic function of the dentate gyrus.

Authors:  C G Dengler; D A Coulter
Journal:  Prog Brain Res       Date:  2016-05-18       Impact factor: 2.453

10.  The spiking component of oscillatory extracellular potentials in the rat hippocampus.

Authors:  Erik W Schomburg; Costas A Anastassiou; György Buzsáki; Christof Koch
Journal:  J Neurosci       Date:  2012-08-22       Impact factor: 6.167

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