Dynamics of Glutamatergic Drive Underlie Diverse Responses of Olfactory Bulb Outputs In Vivo

Mitral/tufted (MT) cells of the olfactory bulb (OB) show diverse temporal responses to odorant stimulation that are thought to encode odor information. Much of this diversity is thought to arise from inhibitory OB circuits, but the dynamics of excitatory input to MT cells, which is driven in a feedforward manner by sensory afferents, may also be important. To examine the contribution of excitatory input dynamics to generating temporal diversity in MT cells, we imaged glutamate signaling onto MT cell dendrites in anesthetized and awake mice. We found surprising diversity in the temporal dynamics of these signals. Inhalation-linked glutamate transients were variable in onset latency and duration, and in awake mice the degree of coupling to inhalation varied substantially with odorant identity and concentration. Successive inhalations of odorant produced nonlinear changes in glutamate signaling that included facilitating, adapting and suppressive responses and which varied with odorant identity and concentration. Dual-color imaging of glutamate and calcium signals from MT cells in the same glomerulus revealed highly correlated presynaptic and postsynaptic signals across these different response types. Suppressive calcium responses in MT cells were nearly always accompanied by suppression in the glutamate signal, providing little evidence for MT cell suppression by lateral or feedforward inhibition. These results indicate a high degree of diversity in the dynamics of excitatory input to MT cells, and suggest that these dynamics may account for much of the diversity in MT cell responses that underlies OB odor representations.