Commissural projection to the dentate gyrus of the rat: evidence for feed-forward inhibition

Buzsáki, György; Eidelberg, E.

doi:10.1016/0006-8993(81)90413-3

Cited by 163 publications

(76 citation statements)

References 13 publications

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“…+ interneurons in microcircuits: Beyond simple inhibition GABAergic interneurons are involved in both feedforward and feedback inhibition (70)(71)(72)(73)Box 3). But what is the specific contribution of PV + cells, and what is the functional relevance of their fast signaling mechanisms?…”

Section: Role Of Pvmentioning

confidence: 99%

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function

Gan

Jónás

2014

Science

1,040

1,001

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Review summary (print version)Background Fast-spiking, parvalbumin-expressing interneurons (PV + interneurons) play a key role in several functions of the brain. They contribute to feedback and feedforward inhibition, and are critically involved in the generation of network oscillations. A hallmark property of these interneurons is speed. In essence, these cells convert an excitatory input signal into an inhibitory output signal within a millisecond. How these remarkable signaling properties are implemented at the molecular and cellular level has been unclear. Furthermore, how PV + interneurons shape complex network functions has remained an open question. Advances Outlook PV+ interneurons may also play a key role in numerous brain diseases. These include epilepsy, but also complex psychiatric diseases, such as schizophrenia. Thus, PV + interneurons may become important therapeutic targets in the future. However, much needs to be learned about the basic function of these interneurons before clinical neuroscientists will have a chance to successfully use PV + interneurons for therapeutic purposes. 3 Full article (online) AbstractThe success story of fast-spiking, parvalbumin-expressing (PV + ) GABAergic interneurons is amazing. In 1995, the properties of these interneurons were completely unknown. 20 years later, thanks to the massive use of subcellular patchclamp techniques, simultaneous multiple-cell recording, optogenetics, in vivo measurements, and computational approaches, our knowledge about PV + interneurons became more extensive than for several types of pyramidal neurons (Box 1). These findings have implications beyond the "small world" of basic research on GABAergic cells. For example, the results provide a first proof of principle that neuroscientists might be able to close the gaps between molecular, cellular, network, and behavioral level, which represents one of the main challenges at the present time. Furthermore, the results may form the basis for using PV + interneurons as therapeutical targets for brain diseases in the future. However, much needs to be learned about the basic function of these interneurons before clinical neuroscientists will be able to use PV + interneurons for therapeutic purposes.

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Section: Role Of Pvmentioning

confidence: 99%

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function

Gan

Jónás

2014

Science

1,040

1,001

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“…These specific cable properties define unique signaling characteristics, promoting phasic activation of BCs by fast EPSPs and at the same time tonic activation by slow distal inputs. This may explain rapid and efficient recruitment of BCs during different forms of network activity, such as feedback inhibition, feedforward inhibition, and high-frequency oscillatory activity (1,3,4,40).…”

Section: )mentioning

confidence: 99%

“…cable models | dendrites | hippocampus | basket cell F ast-spiking, parvalbumin-expressing basket cells (BCs) play an important role in feedforward and feedback inhibition, providing rapid control over the frequency and timing of action potential initiation in principal neuron ensembles (1)(2)(3)(4)(5)(6). Although inhibition comprises several steps, including activation of excitatory input synapses on BCs, dendritic integration of excitatory postsynaptic potentials (EPSPs), action potential initiation and propagation, and GABA release from output synapses, the kinetics of disynaptic inhibition can be very rapid, with ≈2 ms total onset time at physiologic temperature (3,7).…”

mentioning

confidence: 99%

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

Nörenberg

Vida

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

122

166

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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.cable models | dendrites | hippocampus | basket cell F ast-spiking, parvalbumin-expressing basket cells (BCs) play an important role in feedforward and feedback inhibition, providing rapid control over the frequency and timing of action potential initiation in principal neuron ensembles (1-6). Although inhibition comprises several steps, including activation of excitatory input synapses on BCs, dendritic integration of excitatory postsynaptic potentials (EPSPs), action potential initiation and propagation, and GABA release from output synapses, the kinetics of disynaptic inhibition can be very rapid, with ≈2 ms total onset time at physiologic temperature (3, 7). Several synaptic specializations contribute to the remarkable speed of feedforward and feedback inhibition. At the glutamatergic input synapses of BCs, the fast clearance of transmitter from the synaptic cleft and the expression of molecularly specialized L-α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptors (AMPARs) contribute to rapid signaling (8, 9). At the GABAergic output synapses of BCs, the use of rapidly gated P/Qtype Ca 2+ channels and the tight coupling of these channels to the Ca 2+ sensors of exocytosis may serve a similar function (10, 11). Thus, functional specializations at both input and output synapses maximize the speed of BC-mediated disynaptic inhibition.Synaptic location, dendritic structure, and electrical cable properties will also contribute to rapid signaling in GABAergic interneurons. For example, the proximal location of excitatory synapses may promote rapid activation of BCs. The significance of this factor, however, is unclear, because many glutamatergic synapses terminate on distal dendrites of BCs (12). Furthermore, rapid signaling could be promoted by the extensive axon, which may accelerate the somatic EPSP decay time course by ge...

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“…In contrast, the high density of Na + channels in the axon conveys robust analogue-digital conversion and rapid propagation of the digital signal. These cellular properties are expected to be critically important for the function of BCs, which mediate fast feedforward and feedback inhibition in hippocampal microcircuits 2,3 . It is well established that the time required for disynaptic inhibition in microcircuits can be as short as 1 ms 8 .…”

Section: Implications For Microcircuit and Network Functionmentioning

confidence: 99%

“…These interneurons mediate fast feedforward and feedback inhibition [1][2][3] , generate network oscillations in the gamma frequency range [4][5][6] , and contribute to complex information processing in neuronal networks, such as pattern separation 7 . For all of these functions, speed and reliability of signaling of GABAergic interneurons is critically important.…”

Section: Introductionmentioning

confidence: 99%

A supercritical density of fast Na+ channels ensures rapid propagation of action potentials in GABAergic interneuron axons

Hu¹

2013

Intrinsic Act

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Fast-spiking, parvalbumin-expressing GABAergic interneurons/basket cells (BCs) play a key role in feedforward and feedback inhibition, gamma oscillations, and complex information processing. For these functions, fast propagation of action potentials (APs) from the soma to the presynaptic terminals is important. However, the functional properties of interneuron axons remain elusive. Here, we examined interneuron axons by confocally targeted subcellular patch-clamp recording in rat hippocampal slices. APs were initiated in the proximal axon ~20 μm from the soma, and propagated to the distal axon with high reliability and speed. Subcellular mapping revealed a stepwise increase of Na + conductance density from the soma to the proximal axon, followed by a further gradual increase in the distal axon. Active cable modeling and experiments with partial channel block indicated that low axonal Na + conductance density was sufficient for reliability, but high Na + density was necessary for both speed of propagation and fast-spiking AP phenotype. Our results suggest that a supercritical density of Na + channels compensates for the morphological properties of interneuron axons (small segmental diameter, extensive branching, and high bouton density), ensuring fast AP propagation and high-frequency repetitive firing.Fast-spiking, parvalbumin-expressing GABAergic interneurons/BCs play a key role in the function of neuronal networks. These interneurons mediate fast feedforward and feedback inhibition [1][2][3] , generate network oscillations in the gamma frequency range [4][5][6] , and contribute to complex information processing in neuronal networks, such as pattern separation 7 . For all of these functions, speed and reliability of signaling of GABAergic interneurons is critically important. In essence, BCs need to convert an excitatory input signal into an inhibitory output signal within a millisecond or less 8 . Furthermore, BCs need to reliably distribute this output signal onto a large number of target cells 9 . However, the subcellular mechanisms Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms Corresponding authors: Dr. Peter Jonas, Dr. Hua Hu, IST Austria, Am Campus 1, A-3400 Klosterneuburg, Austria, Phone: + +43-2243-9000-3701, Fax: ++43-2243-9000-2007, peter.jonas@ist.ac.at, hua.hu@ist.ac.at. AUTHOR CONTRIBUTIONS H.H. performed experiments and analyzed the data, P.J. performed modeling and wrote the paper. Both authors jointly revised the paper. COMPETING FINANCIAL INTERESTSThe authors declare that they have no competing financial interests. Europe PMC Funders GroupAuthor Manuscript Nat Neurosci. Author manuscript; available in PMC 2015 January 07. Published in final edited form as:Nat Neurosci. 2014 May ; 17(5): 686-693. doi:10.1038/nn.3678. Europe PMC Funders Author ManuscriptsEurope PMC Funders Author Manuscripts un...

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Commissural projection to the dentate gyrus of the rat: evidence for feed-forward inhibition

Cited by 163 publications

References 13 publications

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function

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

A supercritical density of fast Na+ channels ensures rapid propagation of action potentials in GABAergic interneuron axons

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Commissural projection to the dentate gyrus of the rat: evidence for feed-forward inhibition

Cited by 163 publications

References 13 publications

Fast-spiking, parvalbumin + GABAergic interneurons: From cellular design to microcircuit function

Fast-spiking, parvalbumin + GABAergic interneurons: From cellular design to microcircuit function

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

A supercritical density of fast Na+ channels ensures rapid propagation of action potentials in GABAergic interneuron axons

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Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function