Contrasting short‐term plasticity at two sides of the mitral–granule reciprocal synapse in the mammalian olfactory bulb

Abstract

The mitral-granule reciprocal synapse shapes the response of the olfactory bulb to odour stimuli by mediating lateral and reciprocal inhibition. We investigated the short-term plasticity of both the mitral-to-granule excitatory synapse and the granule-to-mitral inhibitory synapse in rat olfactory bulb slices, using whole-cell patch clamp recordings. The granule-to-mitral inhibitory synapse invariably exhibited paired-pulse depression at interstimulus intervals of less than a second, while the mitral-to-granule excitatory synapse showed heterogeneous responses, which on average yielded a moderate facilitation. Trains of stimuli led to a much greater depression at the granule-to-mitral synapse than at the mitral-to-granule synapse. Since mitral cells commonly respond to odours by burst firing with each inhalation cycle, we used bursts of stimuli to study recovery from depression. We found that recovery from depression induced by fast trains of stimuli was more rapid at the mitral-to-granule synapse than at the granule-to-mitral synapse. In addition, depression was enhanced by higher calcium concentrations, suggesting at least partial contribution of presynaptic mechanisms to short-term depression. The observed short-term plasticity could enable mitral cells to overcome autoinhibition and increase action potential propagation along lateral dendrites by burst firing.

Activity-dependent gating of lateral inhibition in the mouse olfactory bulb

“…The large magnitude inhibition observed at high postsynaptic firing rates had a maximum duration of approximately 300 ms. This is consistent with the observation that granule cell-mediated lateral inhibition undergoes synaptic depression during repetitive stimulation 23,27 , and indicates that the strength of lateral inhibition between mitral cells not only depends on the instantaneous levels of pre-and postsynaptic activity, but also on the recent history of activity.…”

“…The large magnitude inhibition observed at high postsynaptic firing rates had a maximum duration of approximately 300 ms. This is consistent with the observation that granule cell-mediated lateral inhibition undergoes synaptic depression during repetitive stimulation 23,27 , and indicates that the strength of lateral inhibition between mitral cells not only depends on the instantaneous levels of pre-and postsynaptic activity, but also on the recent history of activity.As an independent measure of lateral inhibition we also examined the magnitude of recurrent IPSPs recorded in the postsynaptic mitral cell with and without activity of the presynaptic cell. We quantified recurrent inhibition by measuring the hyperpolarization following a 400-ms train of action potentials of a given frequency 28 .…”

“…One difference between our simulations and the data on time-dependent decorrelation is that we did not see examples of patterns of activity evoked by two different odors becoming increasingly correlated across time, as is seen in a subset of cells recorded experimentally 3 . This may be a result of the simplicity of our model, which does not include features such as excitatory coupling between mitral cells 27,34,35 or short-term plasticity of lateral inhibition 23 that may be important for these aspects of the described results. As a demonstration, we also tested this mechanism for specifying lateral inhibition on an image-processing application.…”

“…The IPSPs evoked had a maximum amplitude of <2 mV and typically showed synaptic depression (Fig. 1b) 23 . By injecting current steps of various amplitudes (400 ms, 0-1,200 pA) into the mitral cell, we determined the relationship between firing frequency and injected current (F-I curve) of the postsynaptic mitral cell.…”

“…Spatial integration of excitatory input in the granule cell dendritic tree also could be important 37 . Furthermore, because granule cell-mediated recurrent and lateral inhibition saturate at higher firing rates 23,27,28 , strongly active mitral cells 'immunize' themselves against lateral inhibition by activating a large fraction of the granule cells that provide them with inhibition. The firing rates required for this suppression of inhibition, although high, are observed in vivo in anaesthetized preparations 28,38 .…”