Abstract

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.

Highlights

  • Exploration of neuronal activity in the hippocampus [1] and lesion studies [2] led to the conclusion that the hippocampus is involved in the encoding and recall of spatial information [3,4,5], one form of processing temporal sequences of events

  • We explore how hippocampal GABAergic neuronal activity may change the excitability of pyramidal cells during theta and high-frequency ripple oscillations, two rhythms thought to represent key stages of navigation-related neuronal activity

  • Long periods of awake immobility and consummatory behaviour, the hippocampus displays large amplitude irregular activity containing synchronous population burst of subsets of pyramidal cells and interneurons resulting in a fast oscillation in the pyramidal layer (120–200 Hz), the ripple [5]

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Summary

Introduction

Exploration of neuronal activity in the hippocampus [1] and lesion studies [2] led to the conclusion that the hippocampus is involved in the encoding and recall of spatial information [3,4,5], one form of processing temporal sequences of events. Specific types of interneuron recognized by their shapes from Golgi impregnation [26] or intracellular injection of tracer molecules [27] reflect distinct synaptic relationships to pyramidal cells and can be further specified by the selective localization of molecules involved in intercellular signalling such as neuropeptides, receptors and calcium-binding proteins [28 –30]. For behaviour-related neuronal dynamics, interneuron types defined by their distinct synaptic relationships show remarkable firing specificity during different network states in vivo [17,31]. A set of six types of GABAergic cell, in addition to innervating pyramidal cells and interneurons in the hippocampus, project to extrahippocampal areas such as the septum, subiculum, indusium griseum, retrosplenial cortex and the entorhinal cortex [37,42,43]. It is not yet clear whether all types of CA1 pyramidal cell receive input from all of the interneurons innervating pyramidal cells

Theta oscillation and interneuron firing
Sharp wave-associated ripple oscillations and interneuronal firing
Temporal dynamics of the same GABAergic cell types in CA1 and CA3
Plasticity of interneuron influence and navigation
Outlook
66. Fuentealba P et al 2010 Expression of COUP-TFII
42. Jinno S et al 2007 Neuronal diversity in GABAergic
96. Ferraguti F et al 2005 Metabotropic glutamate
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