Abstract

Hippocampal inhibitory interneurons exhibit a large diversity of dendritic Ca2+ mechanisms that are involved in the induction of Hebbian and anti-Hebbian synaptic plasticity. High resolution imaging techniques allowed examining somatic Ca2+ signals and, accordingly, the recruitment of hippocampal interneurons in awake behaving animals. However, little is still known about dendritic Ca2+ activity in interneurons during different behavioral states. Here, we used two-photon Ca2+ imaging in mouse hippocampal CA1 interneurons to reveal Ca2+ signal patterns in interneuron dendrites during animal locomotion and immobility. Despite overall variability in dendritic Ca2+ transients (CaTs) across different cells and dendritic branches, we report consistent behavior state-dependent organization of Ca2+ signaling in interneurons. As such, spreading regenerative CaTs dominated in dendrites during locomotion, whereas both spreading and localized Ca2+ signals were seen during immobility. Thus, these data indicate that while animal locomotion is associated with widespread Ca2+ elevations in interneuron dendrites that may reflect regenerative activity, local CaTs that may be related to synaptic activity become apparent during animal quiet state.

Highlights

  • Neuronal dendrites exhibit a large variety of voltage- and ligand-gated ion conductances and, may operate as independent signaling devices (Branco and Häusser, 2011)

  • To study dendritic Ca2+ signals in hippocampal interneurons during different behavioral states, we performed chronic two-photon Ca2+ imaging of CA1 O/A interneurons labeled with a genetically-encoded calcium indicator GCaMP6f in head-restrained mice running on a circular treadmill (Figure 1A)

  • Interneurons were identified based on the soma location within CA1 O/A and horizontally oriented dendrites located within the same focal plane (Figure 1B)

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Summary

INTRODUCTION

Neuronal dendrites exhibit a large variety of voltage- and ligand-gated ion conductances and, may operate as independent signaling devices (Branco and Häusser, 2011). Local circuit GABAergic inhibitory interneurons in hippocampal regions control the integration and transfer of information during different network and behavioral states (Klausberger and Somogyi, 2008; Somogyi, 2010; Pelkey et al, 2017) These cells exhibit a large repertoire of voltageand ligand-gated Ca2+ mechanisms, which are regulated differentially by changes in pre- and postsynaptic activity, and provide a means for a highly dynamic and versatile regulation of synaptic plasticity (Topolnik et al, 2005, 2006, 2009; Evstratova et al, 2011; Camiré and Topolnik, 2014; Hainmueller et al, 2014). This statedependent Ca2+ signaling suggests that distinct forms of synaptic plasticity can be induced in interneurons of awake mice during different behavioral states

MATERIALS AND METHODS
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DISCUSSION

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