Functional interaction of electrical coupling and H-current and its putative impact on inhibitory transmission

Abstract

The flow of information within neural circuits depends on the communication between neurons, primarily taking place at chemical and electrical synapses. The coexistence of these two modalities of synaptic transmission and their dynamical interaction with voltage-gated membrane conductances enables a rich repertoire of complex functional operations. One such operation, coincidence detection, allows electrically coupled neurons to respond more strongly to simultaneous synaptic inputs than to temporally dispersed ones. Using the mesencephalic trigeminal (MesV) nucleus—a structure composed of large, somatically coupled neurons—as an experimental model, we first demonstrate that electrical coupling strength in the hyperpolarized voltage range is highly time-dependent due to the involvement of the IH current. We then show how this property influences the coincidence detection of hyperpolarizing signals. Specifically, simultaneous hyperpolarizing inputs induce larger membrane potential changes, resulting in stronger IH current activation. This, in turn, shortens the temporal window for coincidence detection. We propose that this phenomenon may be crucial for networks dynamics in circuits of electrically coupled neurons that receive inhibitory synaptic inputs and express the IH current. In particular, molecular layer interneurons (MLIs) of the cerebellar cortex provide an ideal model for studying coincidence detection of inhibitory synaptic inputs, and how this operation is shaped by the voltage-dependent conductances like the IH current, potentially impacting on motor coordination and learning.