Temporal redistribution of inhibition over neuronal subcellular domains underlies state-dependent rhythmic change of excitability in the hippocampus

The behaviour-contingent rhythmic synchronization of neuronal activity is reported by local field potential oscillations in the theta, gamma and sharp wave-related ripple (SWR) frequency ranges. In the hippocampus, pyramidal cell assemblies representing temporal sequences are coordinated by GABAergi...

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Published in:Philosophical transactions of the Royal Society of London. Series B. Biological sciences 2014-02, Vol.369 (1635), p.20120518-20120518
Main Authors: Somogyi, Peter, Katona, Linda, Klausberger, Thomas, Lasztóczi, Bálint, Viney, Tim J.
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Animals
Axons - physiology
Biological Clocks - physiology
CA1 Region, Hippocampal - cytology
CA1 Region, Hippocampal - physiology
CA3 Region, Hippocampal - cytology
CA3 Region, Hippocampal - physiology
GABA
gamma-Aminobutyric Acid - physiology
Inhibition
Interneuron
Neural Pathways - physiology
Oscillation
Part IV: Oscillatory networks
Parvalbumins - physiology
Pyramidal Cells - physiology
Rats
Review
Synapse
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Summary:The behaviour-contingent rhythmic synchronization of neuronal activity is reported by local field potential oscillations in the theta, gamma and sharp wave-related ripple (SWR) frequency ranges. In the hippocampus, pyramidal cell assemblies representing temporal sequences are coordinated by GABAergic interneurons selectively innervating specific postsynaptic domains, and discharging phase locked to network oscillations. We compare the cellular network dynamics in the CA1 and CA3 areas recorded with or without anaesthesia. All parts of pyramidal cells, except the axon initial segment, receive GABA from multiple interneuron types, each with distinct firing dynamics. The axon initial segment is exclusively innervated by axo-axonic cells, preferentially firing after the peak of the pyramidal layer theta cycle, when pyramidal cells are least active. Axo-axonic cells are inhibited during SWRs, when many pyramidal cells fire synchronously. This dual inverse correlation demonstrates the key inhibitory role of axo-axonic cells. Parvalbumin-expressing basket cells fire phase locked to field gamma activity in both CA1 and CA3, and also strongly increase firing during SWRs, together with dendrite-innervating bistratified cells, phasing pyramidal cell discharge. Subcellular domain-specific GABAergic innervation probably developed for the coordination of multiple glutamatergic inputs on different parts of pyramidal cells through the temporally distinct activity of GABAergic interneurons, which differentially change their firing during different network states.
ISSN:0962-8436
1471-2970
DOI:10.1098/rstb.2012.0518