Drift in neural population activity causes working memory to deteriorate over time

Abstract

Short-term memories are thought to be maintained in the form of sustained spiking activity in neural populations. Decreases in recall precision observed with increasing number of memorized items can be accounted for by a limit on total spiking activity, resulting in fewer spikes contributing to the representation of each individual item. Longer retention intervals likewise reduce recall precision, but it is unknown what changes in population activity produce this effect. One possibility is that spiking activity becomes attenuated over time, such that the same mechanism accounts for both effects of set size and retention duration. Alternatively, reduced performance may be caused by drift in the encoded value over time, without a decrease in overall spiking activity. Human participants of either sex performed a variable-delay cued recall task with a saccadic response, providing a precise measure of recall latency. Based on a spike integration model of decision making, if the effects of set size and retention duration are both caused by decreased spiking activity, we would predict a fixed relationship between recall precision and response latency across conditions. In contrast, the drift hypothesis predicts no systematic changes in latency with increasing delays. Our results show both an increase in latency with set size, and a decrease in response precision with longer delays within each set size, but no systematic increase in latency for increasing delay durations. These results were quantitatively reproduced by a model based on a limited neural resource in which working memories drift rather than decay with time.