Healthy oscillatory coordination is bounded by single-unit computation

Abstract

Oscillations can improve neural coding by grouping action potentials into synchronous windows of activity, but this same effect can harm coding when action potentials become over-synchronized. Diseases ranging from Parkinson’s to epilepsy suggest that oversynchronization leads to pathology, but the precise boundary separating healthy from pathological synchrony remains an open theoretical problem. Here we study a simple model that shows how error in individual cells’ computations is traded for population-level synchronization. To put the in biological terms accessible to the cell we conceive of a “voltage budget” where instantaneous moments of membrane voltage can be partitioned into oscillatory and computational terms. By comparing these budget terms we derive a new set of biologically measurable inequalities that bound healthy from pathological synchrony. Finally, we derive an optimal non-biological algorithm for exchanging computational error with population synchrony.