A biophysical signature of network affiliation and sensory processing in mitral cells

One defining characteristic of the mammalian brain is its neuronal diversity(1). For a given region, substructure or layer and even cell type(2), variability in neuronal morphology and connectivity(2-5) persists. While it is well established that such cellular properties vary considerably according to neuronal type, the significant biophysical diversity of neurons of the same morphological class is typically averaged out and ignored. Here we show that the amplitude of hyperpolarization-evoked membrane potential sag recorded in olfactory bulb mitral cells is an emergent, homotypic property of local networks and sensory information processing. Simultaneous whole-cell recordings from pairs of cells reveal that the amount of hyperpolarization-evoked sag potential and current(6) is stereotypic for mitral cells belonging to the same glomerular circuit. This is corroborated by a mosaic, glomerulus-based pattern of expression of the HCN2 subunit of the hyperpolarization-activated current (I(h)) channel. Furthermore, inter-glomerular differences in both membrane potential sag and HCN2 protein are diminished when sensory input to glomeruli is genetically and globally altered so only one type of odorant receptor is universally expressed(7). We therefore suggest that population diversity in the intrinsic profile of mitral cells reflect functional adaptations of distinct local circuits dedicated to processing subtly different odor-related information.