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J Neurophysiol. 2016 Dec 1;116(6):2564-2575. doi: 10.1152/jn.00413.2016. Epub 2016 Sep 7.

Dynamic balance of excitation and inhibition rapidly modulates spike probability and precision in feed-forward hippocampal circuits.

Author information

1
Departments of Cell Biology & Physiology and Biomedical Engineering, Center for the Investigation of Membrane Excitable Diseases, Washington University School of Medicine, St. Louis, Missouri.
2
Departments of Cell Biology & Physiology and Biomedical Engineering, Center for the Investigation of Membrane Excitable Diseases, Washington University School of Medicine, St. Louis, Missouri klyachko@wustl.edu.

Abstract

Feed-forward inhibitory (FFI) circuits are important for many information-processing functions. FFI circuit operations critically depend on the balance and timing between the excitatory and inhibitory components, which undergo rapid dynamic changes during neural activity due to short-term plasticity (STP) of both components. How dynamic changes in excitation/inhibition (E/I) balance during spike trains influence FFI circuit operations remains poorly understood. In the current study we examined the role of STP in the FFI circuit functions in the mouse hippocampus. Using a coincidence detection paradigm with simultaneous activation of two Schaffer collateral inputs, we found that the spiking probability in the target CA1 neuron was increased while spike precision concomitantly decreased during high-frequency bursts compared with a single spike. Blocking inhibitory synaptic transmission revealed that dynamics of inhibition predominately modulates the spike precision but not the changes in spiking probability, whereas the latter is modulated by the dynamics of excitation. Further analyses combining whole cell recordings and simulations of the FFI circuit suggested that dynamics of the inhibitory circuit component may influence spiking behavior during bursts by broadening the width of excitatory postsynaptic responses and that the strength of this modulation depends on the basal E/I ratio. We verified these predictions using a mouse model of fragile X syndrome, which has an elevated E/I ratio, and found a strongly reduced modulation of postsynaptic response width during bursts. Our results suggest that changes in the dynamics of excitatory and inhibitory circuit components due to STP play important yet distinct roles in modulating the properties of FFI circuits.

KEYWORDS:

feed-forward inhibition; short-term plasticity; synaptic dynamics

PMID:
27605532
PMCID:
PMC5133295
DOI:
10.1152/jn.00413.2016
[Indexed for MEDLINE]
Free PMC Article

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