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Short‐term plasticity regulates the excitation/inhibition ratio and the temporal window for spike integration in CA 1 pyramidal cells
Author(s) -
Bartley Aundrea F.,
Dobrunz Lynn E.
Publication year - 2015
Publication title -
european journal of neuroscience
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.346
H-Index - 206
eISSN - 1460-9568
pISSN - 0953-816X
DOI - 10.1111/ejn.12898
Subject(s) - schaffer collateral , excitatory postsynaptic potential , neuroscience , inhibitory postsynaptic potential , hippocampal formation , chemistry , pyramidal cell , synaptic plasticity , biology , receptor , biochemistry
Many neurodevelopmental and neuropsychiatric disorders involve an imbalance between excitation and inhibition caused by synaptic alterations. The proper excitation/inhibition (E/I) balance is especially critical in CA 1 pyramidal cells, because they control hippocampal output. Activation of Schaffer collateral axons causes direct excitation of CA 1 pyramidal cells, quickly followed by disynaptic feedforward inhibition, stemming from synaptically induced firing of GABA ergic interneurons. Both excitatory and inhibitory synapses are modulated by short‐term plasticity, potentially causing dynamic tuning of the E/I ratio. However, the effects of short‐term plasticity on the E/I ratio in CA 1 pyramidal cells are not yet known. To determine this, we recorded disynaptic inhibitory postsynaptic currents and the E/I ratio in CA 1 pyramidal cells in acute hippocampal slices from juvenile mice. We found that, whereas inhibitory synapses had paired‐pulse depression, disynaptic inhibition instead had paired‐pulse facilitation (≤ 200‐ms intervals), caused by increased recruitment of feedforward interneurons. Although enhanced disynaptic inhibition helped to constrain paired‐pulse facilitation of excitation, the E/I ratio was still larger on the second pulse, increasing pyramidal cell spiking. Surprisingly, this occurred without compromising the precision of spike timing. The E/I balance regulates the temporal spike integration window from multiple inputs; here, we showed that paired‐pulse stimulation can broaden the spike integration window. Together, our findings show that the combined effects of short‐term plasticity of disynaptic inhibition and monosynaptic excitation alter the E/I balance in CA 1 pyramidal cells, leading to dynamic modulation of spike probability and the spike integration window. Short‐term plasticity is therefore an important mechanism for modulating signal processing of hippocampal output.