Disynaptic Amplification of Metabotropic Glutamate Receptor 1 Responses in the Olfactory Bulb

Abstract

Sensory systems often respond to rapid stimuli with high frequency and fidelity, as perhaps best exemplified in the auditory system. Fast synaptic responses are fundamental requirements to achieve this task. The importance of speed is less clear in the olfactory system. Moreover, olfactory bulb output mitral cells respond to a single stimulation of the sensory afferents with unusually long EPSPs, lasting several seconds. We examined the temporal characteristics, developmental regulation, and the mechanism generating these responses in mouse olfactory bulb slices. The slow EPSP appeared at postnatal days 10 -11 and was mediated by metabotropic glutamate receptor 1 (mGluR1) and NMDA receptors. mGluR1 contribution was unexpected because its activation usually requires strong, high-frequency stimulation of inputs. However, dendritic release of glutamate from the intraglomerular network caused spillover-mediated recurrent activation of metabotropic glutamate receptors. We suggest that persistent responses in mitral cells amplify the incoming sensory information and, along with asynchronous inputs, drive odor-evoked slow temporal activity in the bulb.

External Tufted Cells Drive the Output of Olfactory Bulb Glomeruli

“…Some events lacked a buildup period. As shown previously (De Saint Jan and Westbrook, 2007), spontaneous slow currents reversed polarity at positive holding potentials and were blocked by AMPA and NMDA receptor antagonists (10 M NBQX and 50 M D-AP-5, respectively) (data not shown). Also consistent with previous studies (Carlson et al, 2000;Puopolo and Belluzzi, 2001;Schoppa and Westbrook, 2001;De Saint Jan and Westbrook, 2007), spontaneous slow events were synchronized in cells projecting to the same glomerulus (see below) and thus were defined as population bursts.…”

“…Slow glomerulus-specific population bursts, which reflect a synchronized activation of the network, depend on glutamate-mediated transmission (Isaacson, 1999;Carlson et al, 2000;Puopolo and Belluzzi, 2001;Schoppa and Westbrook, 2001;Christie et al, 2005;De Saint Jan and Westbrook, 2007). The pacemaker properties of ET cells result in bursts of APs in synchrony with population bursts in the M-cell ensemble.…”

“…Stimulation of the OSN evokes EPSPs in M cells that have a time course similar to the spontaneous population bursts (Carlson et al, 2000;De Saint Jan and Westbrook, 2007). Thus, we tested whether ET-cell activity contributes to sensory neuronevoked M cell responses.…”

“…Moreover, M cells have the tendency to burst rhythmically within each glomerulus. For instance, increases in the excitability of the bulb network in isolated brain slices induce synchronized population bursts in M cells projecting to the same glomerulus (Isaacson, 1999;Carlson et al, 2000;Puopolo and Belluzzi, 2001;Schoppa and Westbrook, 2001;Christie et al, 2005), which have a time course similar to OSN-evoked M-cell responses (Carlson et al, 2000;De Saint Jan and Westbrook, 2007) and can be entrained by patterned afferent input (Schoppa and Westbrook, 2001).…”

Monosynaptic and Polysynaptic Feed-Forward Inputs to Mitral Cells from Olfactory Sensory Neurons

“…In olfactory bulb slices, a single electrical stimulation of OSNs evokes a complex long-lasting depolarization called LLD in mitral cells (Chen and Shepherd, 1997;Carlson et al, 2000;Schoppa and Westbrook, 2001;De Saint Jan and Westbrook, 2007). This response potentially provides a critical amplification step of the incoming sensory information.…”