Intrinsic neural diversity quenches the dynamic volatility of neural networks

Heterogeneity is the norm in biology. The brain is no different: neuronal cell-types are myriad, reflected through their cellular morphology, type, excitability, connectivity motifs and ion channel distributions. While this biophysical diversity enriches neural systems dynamical repertoire, it remains challenging to reconcile with the robustness and persistence of brain function over time. To better understand the relationship between heterogeneity and resilience, we analyzed both analytically and numerically a non-linear sparse neural network with balanced excitatory and inhibitory connections evolving over long time scales. We examined how neural diversity expressed as excitability heterogeneity in this network influences its dynamic volatility (i.e., its susceptibility to critical transitions). We exposed this network to slowly-varying modulatory fluctuations, continuously interrogating its stability and resilience. Our results show that excitability heterogeneity implements a homeostatic control mechanism tuning network stability in a context-dependent way. Such diversity was also found to enhance network resilience, quenching the volatility of its dynamics, effectively making the system independent of changes in many control parameters, such as population size, connection probability, strength and variability of synaptic weights as well as modulatory drive. Taken together, these results highlight the fundamental role played by cell-type heterogeneity in the robustness of brain function in the face of change. Significance StatementContemporary research has identified widespread cell-to-cell intrinsic diversity in the brain, manifest through variations in biophysical features such as neuronal excitability. A natural question that arises from this phenomenon is what functional role, if any, this heterogeneity might serve. Combining computational and mathematical techniques, this interdisciplinary research shows that intrinsic cell-to-cell diversity, far from mere developmental noise, represents a homeostatic control mechanism, promoting the resilience of neuronal circuits. These results highlight the importance of diversity in the robustness and persistence of brain function over time and in the face of change.