The glomerular layer of the olfactory bulb (OB) contains synaptic connections between olfactory sensory neurons and OB neurons as well as connections among OB neurons. A subpopulation of external tufted cells and periglomerular cells (juxtaglomerular neurons) expresses dopamine, and recent reports suggest that dopamine can inhibit olfactory sensory neuron activation of OB neurons. In this study, whole cell electrophysiological and primary culture techniques were employed to characterize the neuromodulatory properties of dopamine on glutamatergic transmission between rat OB mitral/tufted (M/T) cells and interneurons. Immunocytochemical analysis confirmed the expression of tyrosine hydroxylase, the rate-limiting enzyme for dopamine synthesis, in a subpopulation of cultured neurons. D2 receptor immunoreactivity was also observed in cultured M/T cells. Dopamine reduced spontaneous excitatory synaptic events recorded in interneurons. Although the D1 receptor agonist SKF38393 and the D2 receptor agonist bromocriptine mesylate mimicked this effect, evoked excitatory postsynaptic potentials (EPSPs) recorded from monosynaptically coupled neuron pairs were attenuated by dopamine and bromocriptine but not by SKF38393. Neither glutamate-evoked currents nor the membrane resistance of the postsynaptic interneuron were affected by dopamine. However, evoked calcium channel currents in the presynaptic M/T cell were diminished during the application of either dopamine or bromocriptine, but not SKF38393. Dopamine suppressed calcium channel currents even after nifedipine blockade of L-type channels, suggesting that inhibition of the dihydropyridine-resistant high-voltage activated calcium channels implicated in transmitter release may mediate dopamine's effects on spontaneous and evoked synaptic transmission. Together, these data suggest that dopamine inhibits excitatory neurotransmission between M/T cells and interneurons via a presynaptic mechanism.

Although recent results suggest roles for NMDA and AMPA receptors in odor encoding, little is known about kainate receptors (KARs) in the olfactory bulb (OB). Molecular, immunological, and electrophysiological techniques were used to provide a functional analysis of KARs in the OB. Reverse transcriptase-polymerase chain reaction revealed that the relative level of expression of KAR subunits was GluR5 approximately GluR6 approximately KA2 > KA1 >> GluR7. In situ hybridization data imply that mitral/tufted cells express mostly GluR5 and KA2, whereas interneurons express mostly GluR6 and KA2. Immunohistochemical double-labeling experiments (GluR5/6/7 or GluR5 + synapsin) suggest that KARs are expressed at both synaptic and extrasynaptic loci. This heterogeneous expression of KAR subunits suggests that KARs may play a multitude of roles in odor processing, each tailored to the function of specific OB circuits. A functional analysis, using whole-cell electrophysiology, suggests that one such role is to increase the frequency of glutamate transmission while attenuating the amplitude of individual events, likely via a presynaptic depolarizing mechanism. Such effects would be important to odor processing particularly by OB glomeruli. In these highly compartmentalized structures, an increase in the frequency of glutamate release and the high density of extrasynaptic KARs, activated by spillover, could enhance glomerular synchronization and thus the transfer of more specific sensory information to cortical structures.