Spontaneous field potentials in the glomeruli of the olfactory bulb: The leading role of juxtaglomerular cells

Abstract

Field potentials recorded in the olfactory bulb glomerular layer (GL) are thought to result mainly from activation of mitral and tufted cells. The contribution of juxtaglomerular cells (JG) is unknown. We tested the hypothesis that JG are the main driving force to novel spontaneous glomerular layer field potentials (sGLFPs), which were recorded in rat olfactory bulb slices maintained in an interface chamber. We found that sGLFPs have comparable magnitudes, durations and frequencies both in standard horizontal slices, where all layers with all cell types were present, and in isolated GL slices, where only JG cells were preserved. Hence, the impact of mitral and deep/medium tufted cells to sGLFPs turned out to be minor. Therefore, we propose that the main generators of sGLFPs are JG neurons. We further explored the mechanism of generation of sGLFPs using a neuronal ensemble model comprising all types of cells associated with a single glomerulus. Random orientation and homogenous distribution of dendrites in the glomerular neuropil along with surrounding shell of cell bodies of JG neurons resulted in substantial spatial restriction of the generated field potential. The model predicts that less than 20% of sGLFP can spread from one glomerulus to an adjacent one. The contribution of JG cells to the total field in the center of the glomerulus is estimated as ∼50% ( ∼34% periglomerular and ∼16% external tufted cells), whereas deep/medium tufted cells provide ∼39% and mitral cells only ∼10%. Occasionally, some sGLFPs recorded in adjacent or remote glomeruli were cross-correlated, suggesting involvement of interglomerular communication in information coding. These results demonstrate a leading role of JG cells in activation of the main olfactory bulb (MOB) functional modules. Finally, we hypothesize that the GL is not a set of independent modules, but it represents a subsystem in the MOB network, which can perform initial processing of odors.