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Routing of spike series by dynamic circuits in the hippocampus

Abstract

Recurrent inhibitory loops are simple neuronal circuits found in the central nervous system, yet little is known about the physiological rules governing their activity. Here we use simultaneous somatic and dendritic recordings in rat hippocampal slices to show that during a series of action potentials in pyramidal cells recurrent inhibition rapidly shifts from their soma to the apical dendrites. Two distinct inhibitory circuits are sequentially recruited to produce this shift: one, time-locked with submillisecond precision to the onset of the action potential series, transiently inhibits the somatic and perisomatic regions of pyramidal cells; the other, activated in proportion to the rate of action potentials in the series, durably inhibits the distal apical dendrites. These two operating modes result from the synergy between pre- and postsynaptic properties of excitatory synapses onto recurrent inhibitory neurons with distinct projection patterns. Thus, the onset of a series of action potentials and the rate of action potentials in the series are selectively captured and transformed into different spatial patterns of recurrent inhibition.

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Acknowledgements

We thank B. Gähwiler from the Brain Research Institute of the University of Zürich, where the initial part of the study was performed. We thank J. Anderson for instructions on the use of the camera lucida. We also thank U. Gerber and M. Carandini for critical reading of and L. Glickfeld for comments on the manuscript. This work was supported by the Swiss National Science Foundation and NIH grants.

Author information

Correspondence to Massimo Scanziani.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Methods

Experimental protocols used to test the specificity of Alveus stimulation and to recover the morphology of recorded interneurons. (DOC 21 kb)

Supplementary Figure 1

Recurrent IPSPs are not contaminated by feed-forward IPSPs. (PDF 49 kb)

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Further reading

Figure 1: Shift of recurrent inhibition along the somato-dendritic axis.
Figure 2: Transient activation of somatic and delayed activation of dendritic inhibitory conductances.
Figure 3: Onset-transient and late-persistent interneurons project to distinct layers.
Figure 4: Coincidence detection and integration in onset-transient versus late-persistent interneurons.
Figure 5: Disynaptic inhibition contributes to transience in onset-transient and to delay in late-persistent interneurons.

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