Cellular and network mechanisms of rhythmic recurrent activity in neocortex

Abstract

The neocortex generates periods of recurrent activity, such as the slow (0.1–0.5 Hz) oscillation during slow-wave sleep. Here we demonstrate that slices of ferret neocortex maintained in vitro generate this slow (< 1 Hz) rhythm when placed in a bathing medium that mimics the extracellular ionic composition in situ. This slow oscillation seems to be initiated in layer 5 as an excitatory interaction between pyramidal neurons and propagates through the neocortex. Our results demonstrate that the cerebral cortex generates an ‘up’ or depolarized state through recurrent excitation that is regulated by inhibitory networks, thereby allowing local cortical circuits to enter into temporarily activated and self-maintained excitatory states. The spontaneous generation and failure of this self-excited state may account for the generation of a subset of cortical rhythms during sleep.

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Figure 1: Generation of the slow oscillation in vivo and in vitro.
Figure 2: The slow oscillation is generated first around layer 5 and propagates vertically.
Figure 3: The slow oscillation propagates horizontally.
Figure 4: Local application of glutamate can initiate the slow oscillation.
Figure 5: The slow oscillation can propagate through supragranular layers and depends on excitatory transmission.
Figure 6: The postsynaptic potentials underlying the depolarized state consist of both excitatory and inhibitory events.
Figure 7: The slow oscillation has a refractory period associated with hyperpolarization and decreased excitability.

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Acknowledgements

We thank L. G. Nowak for participation in critical portions of these experiments. We thank L. Nowak, A. Luthi, J. Brumberg, H. Blumenfeld and R. Gallego for comments on the manuscript. This work was supported by the NIH and the McKnight Foundation. For movies and additional information see http://www.mccormicklab.org.

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Correspondence to David A. McCormick.

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Sanchez-Vives, M., McCormick, D. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3, 1027–1034 (2000). https://doi.org/10.1038/79848

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