Distinct temporal filters in mitral cells and external tufted cells of the olfactory bulb

Abstract

Short-term synaptic plasticity is a critical regulator of neural circuits, and largely determines how information is temporally processed. In the olfactory bulb, afferent olfactory receptor neurons respond to increasing concentrations of odorants with barrages of action potentials, and their terminals have an extraordinarily high release probability. These features suggest that during naturalistic stimuli, afferent input to the olfactory bulb is subject to strong synaptic depression, presumably truncating the postsynaptic response to afferent stimuli. To examine this issue, we used single glomerular stimulation in mouse olfactory bulb slices to measure the synaptic dynamics of afferent-evoked input at physiological stimulus frequencies. In cell-attached recordings, mitral cells responded to high frequency stimulation with sustained responses, whereas external tufted cells responded transiently. Consistent with previous reports, olfactory nerve terminals onto both cell types had a high release probability (0.7), from a single pool of slowly recycling vesicles, indicating that the distinct responses of mitral and external tufted cells to high frequency stimulation did not originate presyaptically. Rather, distinct temporal response profiles in mitral cells and external tufted cells could be attributed to slow dendrodendritic responses in mitral cells, as blocking this slow current in mitral cells converted mitral cell responses to a transient response profile, typical of external tufted cells. Our results suggest that despite strong axodendritic synaptic depression, the balance of axodendritic and dendrodendritic circuitry in external tufted cells and mitral cells, respectively, tunes the postsynaptic responses to high frequency, naturalistic stimulation.

Effects of nicotine on regional blood flow in the olfactory bulb in response to olfactory nerve stimulation

“…In olfactory bulb principal neurons, external tufted cells exhibit a lower threshold (higher sensitivity) for excitation compared with mitral cells in response to olfactory sensory inputs [ 29 – 31 ]. In response to high-frequency (50 Hz) olfactory nerve stimulation, mitral cells produce sustained responses, whereas external tufted cells respond transiently [ 32 ]. We therefore speculated that the first peak olfactory bulb blood flow response evoked by olfactory nerve stimulation may reflect external tufted cell excitation, whereas the second peak olfactory bulb blood flow response evoked by high-frequency olfactory nerve stimulation may largely reflect mitral cell excitation.…”

Coding of odors in the anterior olfactory nucleus

“…By contrast to mitral cells, tufted cells are more excitable, and respond with a shorter latency to stimulation of olfactory sensory neurons (Burton & Urban, ; Geramita & Urban, ; Griff, Mafhouz, & Chaput, ; Vaaga & Westbrook, ), hence those that show a clear respiratory rhythm are active earlier in the respiratory cycle than mitral cells, and whereas mitral cells show sustained responses to sensory stimulation, the responses of tufted cells adapt.…”

A dominant role for the beta 4 nicotinic receptor subunit in nicotinic modulation of glomerular microcircuits in the mouse olfactory bulb

“…The results, shown in Table 1, suggest that nAChR modulates both components. If the effect on the fast response corresponds to nAChR-mediated actions on the ON and the slower one on the dendrodendritic circuitry (Vaaga and Westbrook 2017), it could imply that the actions of nAChRs are complex and operative at multiple loci. Countering this conclusion is our finding on ON-ET transmission that remains relatively unaltered by nAChR modulation (D'Souza et al 2013).…”