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.

Bump attractors are localized activity patterns that can self-sustain after stimulus presentation, and they are regarded as the neural substrate for a host of perceptual and cognitive processes. One of the characteristic features of bump attractors is that they are neutrally stable, so that noisy inputs cause them to drift away from their initial locations, severely impairing the accuracy of bump location-dependent neural coding. Previous modeling studies of such noise-induced drifting activity of bump attractors have focused on normal diffusive dynamics, often with an assumption that noisy inputs are uncorrelated. Here we show that long-range temporal correlations and spatial correlations in neural inputs generated by multiple interacting bumps cause them to drift in an anomalous subdiffusive way. This mechanism for generating subdiffusive dynamics of bump attractors is further analyzed based on a generalized Langevin equation. We demonstrate that subdiffusive dynamics can significantly improve the coding accuracy of bump attractors, since the variance of the bump displacement increases sublinearly over time and is much smaller than that of normal diffusion. Furthermore, we reanalyze existing psychophysical data concerning the spread of recalled cue position in spatial working memory tasks and show that its variance increases sublinearly with time, consistent with subdiffusive dynamics of bump attractors. Based on the probability density function of bump position, we also show that the subdiffusive dynamics result in a long-tailed decay of firing rate, greatly extending the duration of persistent activity.