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Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential

Abstract

Traditionally, neuronal operations in the cerebral cortex have been viewed as occurring through the interaction of synaptic potentials in the dendrite and soma, followed by the initiation of an action potential, typically in the axon1,2. Propagation of this action potential to the synaptic terminals is widely believed to be the only form of rapid communication of information between the soma and axonal synapses, and hence to postsynaptic neurons. Here we show that the voltage fluctuations associated with dendrosomatic synaptic activity propagate significant distances along the axon, and that modest changes in the somatic membrane potential of the presynaptic neuron modulate the amplitude and duration of axonal action potentials and, through a Ca2+-dependent mechanism, the average amplitude of the postsynaptic potential evoked by these spikes. These results indicate that synaptic activity in the dendrite and soma controls not only the pattern of action potentials generated, but also the amplitude of the synaptic potentials that these action potentials initiate in local cortical circuits, resulting in synaptic transmission that is a mixture of triggered and graded (analogue) signals.

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Figure 1: Somatic depolarization results in an increase in the amplitude of evoked EPSPs in nearby neurons.
Figure 2: Properties of EPSP enhancement.
Figure 4: Spontaneous barrages of synaptic activity propagate down the axon.
Figure 3: Changes in somatic membrane potential affect the amplitude and duration of somatic and axonal action potentials.

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Acknowledgements

This work was supported by the NIH (D.A.M.), the Howard Hughes Foundation (A.H.) and the Kavli Institute for Neuroscience. Author Contributions Y.S. performed all recordings, A.H. analysed the data, A.D. did cell reconstructions, Y.Y. performed computational models, and D.A.M. wrote the paper and helped design experiments. All authors discussed the results and commented on the manuscript.

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Correspondence to David A. McCormick.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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This file contains the Supplementary Introduction, Supplementary Methods, Supplementary Figures and Supplementary Results. (DOC 800 kb)

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Shu, Y., Hasenstaub, A., Duque, A. et al. Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441, 761–765 (2006). https://doi.org/10.1038/nature04720

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