Stability of electrical coupling despite massive developmental changes of intrinsic neuronal physiology

Gap junctions mediate metabolic and electrical interactions between some cells of the CNS. For many types of neurons, gap junction-mediated electrical coupling is most prevalent during early development, then decreases sharply with maturation. However, neurons in the thalamic reticular nucleus (TRN), which exert powerful inhibitory control over thalamic relay cells, are electrically coupled in relatively mature animals. It is not known whether TRN cells or any neurons that are electrically coupled when mature are also coupled during early development. We used dual whole-cell recordings in mouse brain slices to study the postnatal development of electrical and chemical synapses that interconnect TRN neurons. Inhibitory chemical synapses were seen as early as postnatal day 4 but were infrequent at all ages, whereas TRN cells were extensively connected by electrical synapses from birth onward. Surprisingly, the functional strength of electrical coupling, assayed under steady-state conditions or during spiking, remained relatively constant as the brain matured despite dramatic concurrent changes of intrinsic membrane properties. Most notably, neuronal input resistances declined almost eightfold during the first two postnatal weeks, but there were offsetting increases in gap junctional conductances. This suggests that the size or number of gap junctions increase homeostatically to compensate for leakier nonjunctional membranes. Additionally, we found that the ability of electrical synapses to synchronize high frequency subthreshold signals improved as TRN cells matured. Our results demonstrate that certain central neurons may maintain or even increase their gap junctional communication as they mature.