GABAergic Hub Neurons Orchestrate Synchrony in Developing Hippocampal Networks

By P. Bonifazi, M. Goldin, Michel A. Picardo, I. Jorquera, A. Cattani, Gregory Bianconi, A. Represa, Yehezkel Ben-Ari, Rosa Cossart. Science, 2009

638 citations recorded by the source corpus.

Coordinating Neuronal Assemblies Theoretical models predict the existence of so-called hub neurons—highly connected cells that strongly influence the synchronization of spiking activity in a large group of neurons. However, experimental evidence for the existence of these neuronal hubs is lacking. Bonifazi et al. (p. 1419) used high-resolution, two-photon calcium imaging to measure spontaneous calcium fluctuations in hundreds of neurons simultaneously and determined the relative timing of these fluctuations. Examination of functional connectivity maps, based on temporal correlation measurements, revealed a subpopulation of GABAergic hub neurons displaying a remarkably widespread axonal arborization that orchestrated network synchrony in developing hippocampal networks. Spontaneous network synchronizations in developing hippocampus caused giant depolarizing potentials in individual neurons, and manipulating the spike activity in potential hub cells influenced network activity. A model for the topology of brain networks incorporates a morpho-functional description of neuronal hubs. Brain function operates through the coordinated activation of neuronal assemblies. Graph theory predicts that scale-free topologies, which include “hubs” (superconnected nodes), are an effective design to orchestrate synchronization. Whether hubs are present in neuronal assemblies and coordinate network activity remains unknown. Using network dynamics imaging, online reconstruction of functional connectivity, and targeted whole-cell recordings in rats and mice, we found that developing hippocampal networks follow a scale-free topology, and we demonstrated the existence of functional hubs. Perturbation of a single hub influenced the entire network dynamics. Morphophysiological analysis revealed that hub cells are a subpopulation of γ-aminobutyric acid–releasing (GABAergic) interneurons possessing widespread axonal arborizations. These findings establish a central role for GABAergic interneurons in shaping developing networks and help provide a conceptual framework for studying neuronal synchrony.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/0bc517ccce4f047f59b548c713360359cee7f758

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Citations in the corpus

Neural syntax: cell assemblies, synapsembles and readers (2010, neutral): “Under special conditions, stimulation of a single pyramidal cell or interneuron can recruit a large fraction of neurons in the circuit (Miles, 1990; Bonifazi et al., 2009; Ellender et al., 2010).”
Closed-loop and activity-guided optogenetic control. (2015, positive): “Further, it is important to note that manipulation of local populations with single-cell resolution at the scale made possible by recent published studies is already within the range of the number of neurons that have driven behavioral outcomes in mammals ( 1–50 neurons) in pioneering studies of the”
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition (2010, background): “gained some empirical support from a recent work (94).”
Structured Connectivity in Cerebellar Inhibitory Networks (2014, background): “, 2008) and the presence of hub neurons (Bonifazi et al., 2009).”
Functional connectivity hubs in the human brain (2011, positive): “Studies based on graph theory have documented the scale-free and small-world topologies of the functional connectivity at microscopic level with optical imaging (Bonifazi et al., 2009) and at macroscopic level with magnetic resonance imaging data (Achard et al.”