When animals interact with complex environments, their neural circuits must separate overlapping patterns of activity that represent sensory and motor information. Pattern separation is thought to be a key function of several brain regions, including the cerebellar cortex, insect mushroom body, and dentate gyrus. However, recent findings have questioned long-held ideas on how these circuits perform this fundamental computation. Here, we re-evaluate the functional and structural mechanisms underlying pattern separation. We argue that the dimensionality of the space available for population codes representing sensory and motor information provides a common framework for understanding pattern separation. We then discuss how these three circuits use different strategies to separate activity patterns and facilitate associative learning in the presence of trial-to-trial variability.

Pattern separation is a fundamental function of the brain. The divergent feedforward networks thought to underlie this computation are widespread, yet exhibit remarkably similar sparse synaptic connectivity. Marr-Albus theory postulates that such networks separate overlapping activity patterns by mapping them onto larger numbers of sparsely active neurons. But spatial correlations in synaptic input and those introduced by network connectivity are likely to compromise performance. To investigate the structural and functional determinants of pattern separation we built models of the cerebellar input layer with spatially correlated input patterns, and systematically varied their synaptic connectivity. Performance was quantified by the learning speed of a classifier trained on either the input or output patterns. Our results show that sparse synaptic connectivity is essential for separating spatially correlated input patterns over a wide range of network activity, and that expansion and correlations, rather than sparse activity, are the major determinants of pattern separation.

Highlights d Open Source Brain: an online resource of standardized models of neurons and circuits d Automated 3D visualization, analysis, and simulation of models through the browser d Open source infrastructure and tools for collaborative model development and testing d Accessible, transparent, up-to-date models from different brain regions

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