Modular dynamics of spontaneous activity in neocortex

Yuji Ikegaya, Gloster Aaron and Rafael Yuste

Department of Biological Sciences, Columbia University

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The organization and potential function of the cortical microcircuit are poorly understood. Because spontaneous neuronal activity is prevalent in vivo and in vitro and could reflect intrinsic functional properties of the cortical microcircuit, its dynamics may help reveal basic features of the function and logic of the cortex. In intracellular recordings from a single neuron, we found stereotyped temporal sequences of synaptic inputs that can repeat with millisecond precision even after minutes. These “motifs” seem to represent a fingerprint of the network activity because they concurrently occur in simultaneously recorded pairs of cells, are sensitive to tetrodotoxin, and preferentially emerge during reactivation of the same cells in the same spatiotemporal order, as assessed by calcium imaging from >1000 neurons in slices. Strikingly, series of spatiotemporal sequences are repeated in the same order over tens of seconds. These higher-order sequences (“cortical songs”) are replayed with compressing timing but still maintain their relative temporal relation between the sequences that form them, suggestive of a modular temporal structure of cortical activity. In addition, patterns of spontaneous activity can be predicated by using one past period of data as a training set for a feedback neural network model. Activity patterns during periods that involved more repeated sequences are more accurately predicted. Based on the weighted connections between neurons in a neural network that learned spontaneous activity in datasets, we reconstruct cell assembly organizations in the cortical microcircuit to reveal putative circuit architectures that can produce activity repetitions. Our data demonstrate reverberating patterns of spontaneous activity and underscores the importance of precise temporal dynamics in cortical function.

(Supported by the NEI and the University of Tokyo)

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