Modeling driver cells in developing neuronal networks

Stefano Luccioli (1) , David Angulo-Garcia (2) , Rosa Cossart (3) , Arnaud Malvache (3) , Laura Mòdol (3) , Vitor Hugo Sousa (3) , Paolo Bonifazi (4, 5) , Alessandro Torcini (6, 1, 3)

1 Istituto dei Sistemi Complessi, Consiglio Nazionale delle Ricerche,
2 Departamento de Matematica Aplicada y Estadistica, Universidad Politecnica de Cartagena
3 INMED - INSERM U1249 - Institut de Neurobiologie de la Méditerranée [Aix-Marseille Université]
4 Biocruces Bizkaia Health Research Institute [Baracaldo]
5 Ikerbasque - Basque Foundation for Science
6 LPTM - UMR 8089 - Laboratoire de Physique Théorique et Modélisation

Spontaneous emergence of synchronized population activity is a characteristic feature of developing brain circuits. Recent experiments in the developing neo-cortex showed the existence of driver cells able to impact the synchronization dynamics when single-handedly stimulated. We have developed a spiking network model capable to reproduce the experimental results, thus identifying two classes of driver cells: functional hubs and low functionally connected (LC) neurons. The functional hubs arranged in a clique orchestrated the synchronization build-up, while the LC drivers were lately or not at all recruited in the synchronization process. Notwithstanding, they were able to alter the network state when stimulated by modifying the temporal activation of the functional clique or even its composition. LC drivers can lead either to higher population synchrony or even to the arrest of population dynamics, upon stimulation. Noticeably, some LC driver can display both effects depending on the received stimulus. We show that in the model the presence of inhibitory neurons together with the assumption that younger cells are more excitable and less connected is crucial for the emergence of LC drivers. These results provide a further understanding of the structural-functional mechanisms underlying synchronized firings in developing circuits possibly related to the coordinated activity of cell assemblies in the adult brain. Author summary There is timely interest on the impact of peculiar neurons (driver cells) and of small neuro-nal sub-networks (cliques) on operational brain dynamics. We first provide experimental data concerning the effect of stimulated driver cells on the bursting activity observable in the developing entorhinal cortex. Secondly, we develop a network model able to fully reproduce the experimental observations. Analogously to the experiments two types of driver cells can be identified: functional hubs and low functionally connected (LC) cells. We explain the role of hub neurons, arranged in a clique, for the orchestration of the PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.

Mots clés: Action potentials; Neural networks; Single neuron function; Population dynamics; Depression; Synapses; Neurons; Network analysis

Domaines: Neurosciences [q-bio.NC]

Stefano Luccioli, David Angulo-Garcia, Rosa Cossart, Arnaud Malvache, Laura Mòdol, et al.. Modeling driver cells in developing neuronal networks. PLoS Computational Biology, 2018, 14 (11), pp.e1006551. ⟨10.1371/journal.pcbi.1006551⟩. ⟨hal-01963568⟩