Shunting Inhibition Improves Robustness of Gamma Oscillations in Hippocampal Interneuron Networks by Homogenizing Firing Rates

Vida, Imre; Bartos, Marlene; Jónás, Péter

doi:10.1016/j.neuron.2005.11.036

Cited by 308 publications

(348 citation statements)

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“…Our results show that two distinct types of GABAergic interneuron, PV-expressing basket and ivy cells, the two most numerous GABAergic cell types in the hippocampal pyramidal layer, contribute differentially to behavioral state-dependent neuronal activities and 2,13,15,35,36 through their highly precise inhibitory control of pyramidal cell output 5, 37-39 . They have been predicted to provide a clock-like temporal frame for information coding by pyramidal cells 40 .…”

Section: Discussionmentioning

confidence: 80%

“…So far, an unequivocal recognition of PVexpressing basket cells is only possible by verifying both their molecular expression and axonal arborizations, because PV is expressed also by hippocampal axo-axonic, bistratifed, O-LM and some long-range projection neurons and because other types of basket cell exist which do not express parvalbumin 34 . Parvalbumin-expressing basket cells are thought to contribute to the generation of network oscillations 2,13,15,35,36 through their highly precise inhibitory control of pyramidal cell output 5, 37-39 . They have been predicted to provide a clock-like temporal frame for information coding by pyramidal cells 40 .…”

Section: Discussionmentioning

confidence: 99%

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Behavior-dependent specialization of identified hippocampal interneurons

et al. 2012

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A large variety of GABAergic interneurons control information processing in hippocampal circuits governing the formation of neuronal representations. Whether distinct hippocampal interneuron types contribute differentially to information-processing during behavior is not known. We employed a novel technique for recording and labeling interneurons and pyramidal cells in drug-free, freely-moving rats. Recorded parvalbumin-expressing basket interneurons innervate somata and proximal pyramidal cell dendrites, whereas nitric-oxide-synthase-and neuropeptide-Y-expressing ivy cells provide synaptic and extrasynaptic dendritic modulation. Basket and ivy cells showed distinct spike timing dynamics, firing at different rates and times during theta and ripple oscillations. Basket but not ivy cells changed their firing rates during movement, sleep and quiet wakefulness, suggesting that basket cells coordinate cell assemblies in a behavioral state-contingent manner, whereas persistently-firing ivy cells might control network excitability and homeostasis. Different interneuron types provide GABA to specific subcellular domains at defined times and rates, thus differentially controlling network activity during behavior.GABAergic interneurons control information processing in cortical circuits as percussionists set the rhythm for a melody, or traffic lights regulate the movement of cars through a city. Interneurons generate oscillatory activity 1, 2 , synchronize the activity of pyramidal cells 3 and set time windows for synaptic integration 4 . A large diversity of interneuronal types is a hallmark of cortical circuits. Different domains of pyramidal cells, such as the soma, axoninitial-segment, proximal or distal dendrites 5 are innervated by distinct types of GABAergic interneuron. They also have distinct inputs and membrane properties 6-10 and show different firing patterns during network oscillations induced in vitro [11][12][13][14] or recorded in anesthetized animals 15 , indicating distinct roles for specific interneuron types. However, research on interneurons in drug-free animals that can freely change their behavior, has so far been limited to recordings from unidentified interneurons because of technical limitations. In the barrel cortex of head-restrained mice, groups of interneurons with distinct membrane dynamics during different behavioral states have been described 16,17 and in the hippocampus unidentified interneurons or interneurons belonging to heterogeneous groups expressing parvalbumin and/or somatostatin have been reported [18][19][20][21] to fire with different firing patterns during network oscillations. But, how do specific types of identified interneurons control the activity of cortical circuits in freely-moving animals? CouldCorrespondence and requests for materials should be addressed to D.L. (damien.lapray@pharm.ox.ac.uk) Results Identification of neurons recorded in freely-moving ratsWe recorded the activity of parvalbumin (PV)-expressing basket, ivy and pyramidal cells in the dorsal CA...

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Section: Discussionmentioning

confidence: 80%

Section: Discussionmentioning

confidence: 99%

Behavior-dependent specialization of identified hippocampal interneurons

et al. 2012

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“…It is a pentameric receptor that selectively conducts anions, particularly chloride ions. The activation of GABA A receptors generally causes hyperpolarization of the neuron and shunting inhibition, [115][116][117] which diminishes the chance of a successful firing of action potentials. 118,119 Different anesthetics preferentially target different neurotransmitter receptors.…”

Section: General Anesthetics and The Neural Substrates Of Memorymentioning

confidence: 99%

Inhibition de l’apprentissage et de la mémoire par les anesthésiques généraux

Wang

Orser

2010

Can J Anesth/J Can Anesth

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“…For example, a low value of R m , which may be generated by a high density of leak channels (23), would accelerate the decay of EPSPs by speeding up the membrane time constant. Similarly, a low R i value, which may be caused by a high intracellular Cl -concentration in BCs (24), could accelerate dendrosomatic propagation of synaptic signals.…”

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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.

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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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Shunting Inhibition Improves Robustness of Gamma Oscillations in Hippocampal Interneuron Networks by Homogenizing Firing Rates

Cited by 308 publications

References 62 publications

Behavior-dependent specialization of identified hippocampal interneurons

Behavior-dependent specialization of identified hippocampal interneurons

Inhibition de l’apprentissage et de la mémoire par les anesthésiques généraux

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

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