D-type K+ current controls the function of electrically coupled neurons in a species-specific fashion

Electrical synapses supported by gap junctions, are known to form networks of electrically coupled neurons in many regions of the mammalian brain, where they play relevant functional roles. Yet, how electrical coupling support sophisticated network operations, and the contribution of the intrinsic electrophysiological properties of neurons to these operations, remains incompletely understood. Here, comparative analysis of electrically coupled mesencephalic trigeminal (MesV) neurons, uncovered remarkable difference in the operation of these networks in highly related species. While spiking of MesV neurons might support the recruitment of coupled cells in rats, this rarely occurs in mice. Using whole-cell recordings, we determined that the higher efficacy in postsynaptic recruitment in rats MesV neurons does not result from coupling strength of larger magnitude, but instead from the higher excitability of coupled neurons. Consistently, MesV neurons from rats present a lower threshold current for activation, more hyperpolarized firing level as well as a higher ability to generate repetitive discharges, in comparison to their counterparts from mice. This difference in neuronal excitability results from a significantly higher magnitude of the D-type K+ current (ID) in MesV neurons from mice, indicating that the expression level of this current gates the recruitment of postsynaptic coupled neurons. Since MesV neurons are primary afferents critically involved in the organization of orofacial behaviors, such mechanism might support lateral excitation, by which activation of single neurons at the periphery can spread to coupled partners. Thus, by amplifying sensory inputs, lateral excitation may significantly contribute to information processing and organization of motor outputs.