Network instability dynamics drive a transient bursting period in the developing hippocampus in vivo

Author:

Graf Jürgen1ORCID,Rahmati Vahid123ORCID,Majoros Myrtill1,Witte Otto W1,Geis Christian12ORCID,Kiebel Stefan J3ORCID,Holthoff Knut1,Kirmse Knut14ORCID

Affiliation:

1. Department of Neurology, Jena University Hospital

2. Section Translational Neuroimmunology, Jena University Hospital

3. Department of Psychology, Technical University Dresden

4. Department of Neurophysiology, Institute of Physiology, University of Würzburg

Abstract

Spontaneous correlated activity is a universal hallmark of immature neural circuits. However, the cellular dynamics and intrinsic mechanisms underlying network burstiness in the intact developing brain are largely unknown. Here, we use two-photon Ca2+ imaging to comprehensively map the developmental trajectories of spontaneous network activity in the hippocampal area CA1 of mice in vivo. We unexpectedly find that network burstiness peaks after the developmental emergence of effective synaptic inhibition in the second postnatal week. We demonstrate that the enhanced network burstiness reflects an increased functional coupling of individual neurons to local population activity. However, pairwise neuronal correlations are low, and network bursts (NBs) recruit CA1 pyramidal cells in a virtually random manner. Using a dynamic systems modeling approach, we reconcile these experimental findings and identify network bi-stability as a potential regime underlying network burstiness at this age. Our analyses reveal an important role of synaptic input characteristics and network instability dynamics for NB generation. Collectively, our data suggest a mechanism, whereby developing CA1 performs extensive input-discrimination learning prior to the onset of environmental exploration.

Funder

Deutsche Forschungsgemeinschaft

University of Wuerzburg

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference98 articles.

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