Neuronal Circuits Underlying Persistent Representations Despite Time Varying Activity

Background: Our brains are capable of remarkably stable stimulus representations despite time-varying neural activity. For instance, during delay periods in working memory tasks, while stimuli are represented in working memory, neurons in the prefrontal cortex, thought to support the memory representation, exhibit time-varying neuronal activity. Since neuronal activity encodes the stimulus, its time-varying dynamics appears to be paradoxical and incompatible with stable network stimulus representations. Indeed, this finding raises a fundamental question: can stable representations only be encoded with stable neural activity, or, its corollary, is every change in activity a sign of change in stimulus representation? Results: Here we explain how different time-varying representations offered by individual neurons can be woven together to form a coherent, time-invariant, representation. Motivated by two ubiquitous features of the neocortex-redundancy of neural representation and sparse intracortical connections-we derive a network architecture that resolves the apparent contradiction between representation stability and changing neural activity. Unexpectedly, this network architecture exhibits many structural properties that have been measured in cortical sensory areas. In particular, we can account for few-neuron motifs, synapse weight distribution, and the relations between neuronal functional properties and connection probability. Conclusions: We show that the intuition regarding network stimulus representation, typically derived from considering single neurons, may be misleading and that time-varying activity of distributed representation in cortical circuits does not necessarily imply that the network explicitly encodes time-varying properties.