In the olfactory bulb the sets of mitral cells that project their apical dendrite to the same glomerulus represent unique functional networks. While it is known that mitral cells release vesicular glutamate from their apical tuft it is believed that the resultant self-excitation (SE), transmitted via dendritic gap junctions, is the main form of lateral transmission within the mitral cell assembly. In this study we used simultaneous whole-cell recordings from mitral cell pairs to show that a direct form of chemical lateral excitation (LE) provides a means of mitral cell-mitral cell communication. In contrast to the ubiquitous expression and robust nature of SE, the efficacy of glutamatergic LE between mitral cells is highly variable and mediated by calcium-impermeable AMPA receptors. We also find that the strength of LE is bi-directionally modulated, in a homeostatic manner, by sniffing-like patterns of presynaptic activity. Since these changes last many minutes we suggest that such mitral cell-mitral cell interactions provide the glomerular network with a locus for olfactory plasticity and a potential mechanism for receptive field modulation.