Perisomatic Feedback Inhibition Underlies Cholinergically Induced Fast Network Oscillations in the Rat Hippocampus In Vitro

Mann, Edward O.; Suckling, Jillian M.; Hájos, Norbert; Greenfield, Susan; Paulsen, Ole

doi:10.1016/j.neuron.2004.12.016

Cited by 297 publications

(323 citation statements)

References 42 publications

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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%

“…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.…”

Section: Introductionmentioning

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%

Section: Introductionmentioning

confidence: 99%

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Behavior-dependent specialization of identified hippocampal interneurons

et al. 2012

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“…The positive potential in the extracellular recordings is caused by a positive charge flowing out of the cell, a process called the "source" in current source density analysis [23,24] . Whether the source is an active or passive process depends on the intracellular recording of the soma; if this recording shows a hyperpolarized current (IPSC) coinciding with the source, then the source is likely to be active [25] because hyperpolarization is caused by Cl -influx. In contrast, the negative field potential in the stratum radium (neuronal dendrite location) is due to the positive charge flowing into the dendrite.…”

Section: Discussionmentioning

confidence: 99%

Temperature- and concentration-dependence of kainate-induced γ oscillation in rat hippocampal slices under submerged condition

Wang

Zhou

et al. 2012

Acta Pharmacol Sin

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Aim: Fast neuronal network oscillation at the γ frequency band (γ oscillation: 30-80 Hz) has been studied extensively in hippocampal slices under interface recording condition. The aim of this study is to establish a method for recording γ oscillation in submerged hippocampal slices that allows simultaneously monitoring γ oscillation and the oscillation-related intracellular events, such as intracellular Ca 2+ concentration or mitochondrial membrane potentials. Methods: Horizontal hippocampal slices (thickness: 300 μm) of adult rats were prepared and placed in a submerged or an interface chamber. Extracellular field recordings were made in the CA3c pyramidal layer of the slices. Kainate, an AMPA/kainate receptor agonist, was applied via perfusion. Data analysis was performed off-line. Results: Addition of kainate (25-1000 nmol/L) induced γ oscillation in both the submerged and interface slices. Kainate increased the γ power in a concentration-dependent manner, but the duration of steady state oscillation was reduced at higher concentrations of kainate. Long-lasting γ oscillation was maintained at the concentrations of 100-300 nmol/L. Under submerged condition, γ oscillation was temperature-dependent, with the maximum power achieved at 29 ºC. The induction of γ oscillation under submerged condition also required a fast rate of perfusion (5-7 mL/min) and showed a fast dynamic during development and after the washout. Conclusion: The kainite-induced γ oscillation recorded in submerged rat hippocampal slices is useful for studying the intracellular events related to neuronal network activities and may represent a model to reveal the mechanisms underlying the normal neuronal synchronizations and diseased conditions.

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“…Furthermore, the idea of short-circuiting pyramidal cell axons in order to explain ripple oscillations goes against the established principle that the PC population activity carries highly specific representational information. A second model proposes a feedback loop among PCs and inhibitory neurons [3,1 5,28,40] similar to the mechanism proposed for gamma oscillation generation [43,44]. The problem with this scenario is that the frequency of this mechanism can not be up-scaled to the ripple range [40].…”

Section: Introductionmentioning

confidence: 99%