Towards the cellular substrate of anisotropic lateral inhibition between rat olfactory bulb glomeruli

Sensory systems deploy diverse strategies for discriminating similar stimuli. For instance, spatially isotropic lateral inhibition between neurons showing overlapping receptive fields allows contrast enhancement of primary stimulus representations in the visual system. In the olfactory bulb (OB), odorant identity is primarily represented as a spatially discontinuous map of activated glomeruli. Prior observations on mixture inhibition across glomeruli led us to hypothesize that so-called superficial short-axon-cells -a sub-population of GABAergic/dopaminergic juxtaglomerular cells- underlie a targeted -and thus anisotropic- form of lateral inhibition. Using acute horizontal OB slices from juvenile transgenic rats expressing GFP under control of the tyrosine hydroxylase (TH) promoter, TH/GFP+ cells were targeted for whole-cell recordings using a two-photon microscope, followed by morphological recovery using biocytin-DAB stains (n = 62). We identified two classes of juxtaglomerular TH/GFP+ cells, that could be differentiated by various electrophysiological and morphological characteristics. One class were most likely immature neurons; the second class was more elaborate but clearly different from the juxtaglomerular dopaminergic clasping cells we had identified earlier, with non-adapting spiking and intraglomerular dendritic projections. Stimulation of the olfactory nerve (n = 15) triggered polysynaptic excitatory postsynaptic potentials in all these cells, possibly originating from the intraglomerular network. Cells exhibited thin, long-range axons, spanning for several (4-6) glomeruli (n = 13). Reconstruction of both glomeruli and axons (n = 3 cells) showed a clearly anisotropic glomerular innervation pattern. Thus, these TH/GFP+ cells could in fact constitute the cellular substrate for implementing anisotropic, directed lateral inhibition within the glomerular layer.