A framework for macroscopic phase-resetting curves for generalised spiking neural networks

Brain rhythms emerge from synchronization among interconnected spiking neurons. Key properties of such rhythms can be gleaned from the phase-resetting curve (PRC). Inferring the PRC and developing a systematic phase reduction theory for large-scale brain rhythms remains an outstanding challenge. Here we present a theoretical framework and methodology to compute the PRC of generic spiking networks with emergent collective oscillations. We adopt a renewal approach where neurons are described by the time since their last action potential, a description that can reproduce the dynamical feature of many cell types. For a sufficiently large number of neurons, the network dynamics are well captured by a continuity equation known as the refractory density equation. We develop an adjoint method for this equation giving a semi-analytical expression of the infinitesimal PRC. We confirm the validity of our framework for specific examples of neural networks. Our theoretical framework can link key biological properties at the individual neuron scale and the macroscopic oscillatory network properties. Beyond spiking networks, the approach is applicable to a broad class of systems that can be described by renewal processes.Author summary: The formation of oscillatory neuronal assemblies at the network level has been hypothesized to be fundamental to many cognitive and motor functions. One prominent tool to understand the dynamics of oscillatory activity response to stimuli, and hence the neural code for which it is a substrate, is a nonlinear measure called Phase-Resetting Curve (PRC). At the network scale, the PRC defines the measure of how a given synaptic input perturbs the timing of next upcoming volley of spike assemblies: either advancing or delaying this timing. As a further application, one can use PRCs to make unambiguous predictions about whether communicating networks of neurons will phase-lock as it is often observed across the cortical areas and what would be this stable phase-configuration: synchronous, asynchronous or with asymmetric phase-shifts. The latter configuration also implies a preferential flow of information form the leading network to the follower, thereby giving causal signatures of directed functional connectivity. Because of the key position of the PRC in studying synchrony, information flow and entrainment to external forcing, it is crucial to move toward a theory that allows to compute the PRCs of network-wide oscillations not only for a restricted class of models, as has been done in the past, but to network descriptions that are generalized and can reflect flexibly single cell properties. In this manuscript, we tackle this issue by showing how the PRC for network oscillations can be computed using the adjoint systems of partial differential equations that define the dynamics of the neural activity density.