How neuronal morphology impacts the synchronisation state of neuronal networks

Abstract

AbstractThe biophysical properties of neurons not only affect how information is processed within cells, they can also impact the dynamical states of the network. Specifically, the cellular dynamics of action-potential generation have shown relevance for setting the (de)synchronisation state of the network. The dynamics of tonically spiking neurons typically fall into one of three qualitatively distinct types that arise from distinct mathematical bifurcations of voltage dynamics at the onset of spiking. Accordingly, changes in ion channel composition or even external factors, like temperature, have been demonstrated to switch network behaviour via changes in the spike onset bifurcation and hence its associated dynamical type. A thus far less addressed modulator of neuronal dynamics is cellular morphology. Based on simplified and anatomically realistic mathematical neuron models, we show here that the extent of dendritic arborisation has an influence on the neuronal dynamical spiking type and therefore on the (de)synchronisation state of the network. Specifically, larger dendritic trees prime neuronal dynamics for in-phase-synchronised or splayed-out activity in weakly coupled networks, in contrast to cells with otherwise identical properties yet smaller dendrites. Our biophysical insights hold for generic multicompartmental classes of spiking neuron models (from ball-and-stick-type to anatomically reconstructed models) and establish a direct mechanistic link between neuronal morphology and the susceptibility of neural tissue to synchronisation in health and disease.Significance StatementCellular morphology varies widely across different cell types and brain areas. In this study, we provide a mechanistic link between neuronal morphology and the dynamics of electrical activity arising at the network level. Based on mathematical modelling, we demonstrate that modifications of the size of dendritic arbours alone suffice to switch the behaviour of otherwise identical networks from synchronised to asynchronous activity. Specifically, neurons with larger dendritic trees tend to produce more stable phase relations of spiking across neurons. Given the generality of the approach, we provide a novel, morphology-based hypothesis that explains the differential sensitivity of tissue to epilepsy in different brain areas and assigns relevance to cellular morphology in healthy network computation.