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Turning on and off recurrent balanced cortical activity

Abstract

The vast majority of synaptic connections onto neurons in the cerebral cortex arise from other cortical neurons, both excitatory and inhibitory, forming local and distant ‘recurrent’ networks. Although this is a basic theme of cortical organization, its study has been limited largely to theoretical investigations, which predict that local recurrent networks show a proportionality or balance between recurrent excitation and inhibition, allowing the generation of stable periods of activity1,2,3,4,5. This recurrent activity might underlie such diverse operations as short-term memory4,6,7, the modulation of neuronal excitability with attention8,9, and the generation of spontaneous activity during sleep5,10,11,12,13,14. Here we show that local cortical circuits do indeed operate through a proportional balance of excitation and inhibition generated through local recurrent connections, and that the operation of such circuits can generate self-sustaining activity that can be turned on and off by synaptic inputs. These results confirm the long-hypothesized role of recurrent activity as a basic operation of the cerebral cortex.

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Figure 1: Prefrontal cortical slices generate periods of recurrent activity both spontaneously and in response to electrical stimulation of the neuropil.
Figure 4: The UP state enhances neuronal responses to PSPs in pyramidal cells.
Figure 2: Recurrent activity is generated by a balanced barrage of IPSPs and EPSPs.
Figure 3: The UP state enhances neuronal responses to PSPs in FS interneurons.
Figure 5: Reversal potential of evoked responses for the start and stop stimuli.

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Acknowledgements

We thank R. Yuste for his comments. This work was supported by the National Institutes of Health (D.A.M.), the Human Frontier Science Program (D.A.M.), and by a fellowship from the Howard Hughes Institute (A.H.).

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Correspondence to David A. McCormick.

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Shu, Y., Hasenstaub, A. & McCormick, D. Turning on and off recurrent balanced cortical activity. Nature 423, 288–293 (2003). https://doi.org/10.1038/nature01616

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