Self-organization of nonlinearly coupled neural fluctuations into synergistic population codes

Abstract: Neural activity in the brain exhibits correlated fluctuations that may strongly influence the properties of neural population coding. However, how such correlated neural fluctuations may arise from the intrinsic neural circuit dynamics and subsequently affect the computational properties of neural population activity remains poorly understood. The main difficulty lies in resolving the nonlinear coupling between correlated fluctuations with the overall dynamics of the system. In this study, we investigate the emergence of synergistic neural population codes from the intrinsic dynamics of correlated neural fluctuations in a neural circuit model capturing realistic nonlinear noise coupling of spiking neurons. We show that a rich repertoire of spatial correlation patterns naturally emerges in a bump attractor network and further reveals the dynamical regime under which the interplay between differential and noise correlations leads to synergistic codes. Moreover, we find that negative correlations may induce stable bound states between two bumps, a phenomenon previously unobserved in firing rate models. These noise-induced effects of bump attractors lead to a number of computational advantages including enhanced working memory capacity and efficient spatiotemporal multiplexing and can account for a range of cognitive and behavioral phenomena related to working memory. This study offers a dynamical approach to investigating realistic correlated neural fluctuations and insights to their roles in cortical computations.