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Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex

Abstract

Paired whole-cell voltage recordings were made from synaptically connected spiny stellate neurons in layer 4 of the barrel field in young (P14) rat somatosensory cortex. When postsynaptic action potentials (APs) followed each of 5 presynaptic APs in a 10- or 20-Hz train by less than 25 ms, subsequent unitary EPSP amplitudes were persistently reduced. Induction of long-term depression (LTD) depended on activation of group II metabotropic glutamate receptors, but not on NMDA or AMPA receptors. Reducing postsynaptic increases in intracellular calcium ([Ca2+]i) by intracellular loading with a fast- (BAPTA) or a slow- (EGTA) acting Ca2+ buffer blocked synaptic depression. Analysis of EPSP failures suggested mediation of LTD by a reduction in release probability. We propose a mechanism by which coincident activity results in long-lasting reduction of synaptic efficacy between synaptically connected neurons.

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Figure 1: Pairing of pre- and postsynaptic activity in synaptically coupled excitatory neurons of rat barrel cortex induces a long lasting decrease in EPSPs in L4 spiny stellate neurons.
Figure 2: LTD following correlated activity is specific for L4 spiny neuron connections: pairing leads to LTP in L2/3 pyramidal neuron pairs in the same preparation.
Figure 3: Time window of pairing effect: separation of pre- and postsynaptic activity and time window for coincidence and its dependence on AP train frequency.
Figure 4: Calcium dependence and glutamate receptor block.
Figure 5: Binomial analysis before and after pairing: marked increase in failures suggests a presynaptic mechanism in LTD induction.
Figure 6: A functional implication of activity-dependent reduction of EPSP amplitude in spiny stellate cells (a) Amplitude of each EPSP in a pair of spiny stellate cells is plotted against time.

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Acknowledgements

V.E. was supported by the graduate program for molecular and cellular neurobiology, Heidelberg. We thank T. Margrie, M. Larkum and C. Petersen for discussion and comments on the manuscript.

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Correspondence to Dirk Feldmeyer.

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Egger, V., Feldmeyer, D. & Sakmann, B. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat Neurosci 2, 1098–1105 (1999). https://doi.org/10.1038/16026

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