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Short-term depression and transient memory in sensory cortex

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Abstract

Persistent neuronal activity is usually studied in the context of short-term memory localized in central cortical areas. Recent studies show that early sensory areas also can have persistent representations of stimuli which emerge quickly (over tens of milliseconds) and decay slowly (over seconds). Traditional positive feedback models cannot explain sensory persistence for at least two reasons: (i) They show attractor dynamics, with transient perturbations resulting in a quasi-permanent change of system state, whereas sensory systems return to the original state after a transient. (ii) As we show, those positive feedback models which decay to baseline lose their persistence when their recurrent connections are subject to short-term depression, a common property of excitatory connections in early sensory areas. Dual time constant network behavior has also been implemented by nonlinear afferents producing a large transient input followed by much smaller steady state input. We show that such networks require unphysiologically large onset transients to produce the rise and decay observed in sensory areas. Our study explores how memory and persistence can be implemented in another model class, derivative feedback networks. We show that these networks can operate with two vastly different time courses, changing their state quickly when new information is coming in but retaining it for a long time, and that these capabilities are robust to short-term depression. Specifically, derivative feedback networks with short-term depression that acts differentially on positive and negative feedback projections are capable of dynamically changing their time constant, thus allowing fast onset and slow decay of responses without requiring unrealistically large input transients.

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Acknowledgements

We thank Daniel Jeck and Brian Hu for many useful discussions. We would also like to thank Philip O’Herron for help in accessing the physiological data.

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Correspondence to Ernst Niebur.

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The authors declare that they have no conflict of interest.

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Action Editor: Mark Goldman

This work is supported by the Hertz Foundation George Lerman Fellowship and the National Institutes of Health under grant R01DA040990.

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Gillary, G., Heydt, R. & Niebur, E. Short-term depression and transient memory in sensory cortex. J Comput Neurosci 43, 273–294 (2017). https://doi.org/10.1007/s10827-017-0662-8

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  • DOI: https://doi.org/10.1007/s10827-017-0662-8

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