Correlated neural variability in persistent state networks

Abstract

Neural activity that persists long after stimulus presentation is a biological correlate of short-term memory. Variability in spiking activity causes persistent states to drift over time, ultimately degrading memory. Models of short-term memory often assume that the input fluctuations to neural populations are independent across cells, a feature that attenuates population-level variability and stabilizes persistent activity. However, this assumption is at odds with experimental recordings frompairs of cortical neurons showing that both the input currents and output spike trains are correlated. It remains unclear how correlated variability affects the stability of persistent activity and the performance of cognitive tasks that it supports. We consider the stochastic long-timescale attractor dynamics of pairs of mutually inhibitory populations of spiking neurons. In these networks, persistent activity was less variable when correlated variability was globally distributed across both populations compared with the case when correlations were locally distributed only within each population. Using a reduced firing rate model with a continuum of persistent states, we show that, when input fluctuations are correlated across both populations, they drive firing rate fluctuations orthogonal to the persistent state attractor, thereby causing minimal stochastic drift. Using these insights, we establish that distributing correlated fluctuations globally as opposed to locally improves network's performance on a two-interval, delayed response discrimination task. Our work shows that the correlation structure of input fluctuations to a network is an important factor when determining long-timescale, persistent population spiking activity.