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Strong perisomatic inhibition by fast-spiking basket cells (FS-BCs) regulates dentatethroughput. Homotypic FS-BC interconnections that support gamma oscillations, and heterotypicinputs from diverse groups of interneurons that receive extensive neurochemical regulation,together, shape FS-BC activity patterns. However, whether seizures precipitate functionalchanges in inhibitory networks and contribute to abnormal network activity in epilepsy is notknown. In the first recordings from dentate interneuronal pairs in a model of temporal lobeepilepsy, we demonstrate that status epilepticus (SE) selectively compromises GABA release atsynapses from dentate accommodating interneurons (AC-INs) to FS-BCs, while efficacy ofhomotypic FS-BC synapses is unaltered. The functional decrease in heterotypic cannabinoidreceptor type 1 (CB 1 R)-sensitive inhibition of FS-BCs resulted from enhancedbaseline GABA B -mediated suppression of synaptic release after SE. The frequency ofCB 1 R-sensitive inhibitory synaptic events in FS-BCs was depressed early after SEinduction and remained reduced in epileptic rats. In biologically based simulations ofheterogeneous inhibitory networks and excitatory–inhibitory cell networks, experimentallyidentified decrease in reliability of AC-IN to FS-BCs synaptic release reduced theta power andtheta-gamma coupling and enhanced gamma coherence. Thus, the experimentally identifiedfunctional reduction in heterotypic inhibition of FS-BCs can contribute to compromised networkoscillations in epilepsy and could precipitate memory and cognitive co-morbidities.

Functional Reduction in Cannabinoid-Sensitive Heterotypic Inhibition of Dentate Basket Cells in Epilepsy: Impact on Network Rhythms