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Activity-dependent gating of lateral inhibition by correlated mitral cell activity in the mouse main olfactory bulb

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Excitatory mitral and tufted cells (M/Ts) provide the primary output of the mouse main olfactory bulb (MOB). M/Ts provide excitatory input to and receive inhibitory input from GCs via the dendrodendritic synaptic connections. These circuits provide both recurrent and lateral inhibition among M/Ts. However, given the large area spanned by M/T secondary dendrites as well as the lack of evidence for a clear correlation between the proximity of M/Ts and their odor response profiles, we asked what mechanism could provide for specific and useful lateral inhibitory connectivity? To address this question we conducted whole-cell patch clamp recordings of pairs of M/Ts in the MOB. Current steps (400 ms, 0–1200 pA) were injected into one of the paired cells (Cell A). We then compared the firing rate of Cell A when it was stimulated alone vs. when it was stimulated during simultaneous activation of a second M/T (Cell B) at approximately 80 Hz. We found that activity of Cell B significantly reduced the firing rate of Cell A only when Cell A was firing at frequencies between 35 and 110 Hz (19%/17 Hz peak reduction, n = 16 pairs, p < 0.05). This effect, which we call activity-dependent lateral inhibition, is presumably due to activation of GCs correlated M/T cell activity and subsequent saturation of GC output. Furthermore, activation of larger populations of presynaptic M/Ts via extracellular stimulation in the glomerular layer produced similar activity-dependent lateral inhibition but of higher magnitude and occurring at lower frequencies (25% peak reduction between postsynaptic firing rates between 25 and 65 Hz, n = 8, p < 0.05). We then implemented this physiologically characterized mechanism in a network model with all-to-all connectivity. Results show that initially correlated patterns of activity are decorrelated in a spatially independent manner using this activity-dependent mechanism. These results suggest that the magnitude of inhibition received by M/Ts is dynamically determined based on the pattern of activity within the bulb and can be used to decorrelate similar input patterns, enhancing odor discrimination. Supported by R01 – DC005798.

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Correspondence to Nathaniel N Urban.

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Open Access This article is published under license to BioMed Central Ltd. This is an Open Access article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Arevian, A.C., Urban, N.N. Activity-dependent gating of lateral inhibition by correlated mitral cell activity in the mouse main olfactory bulb. BMC Neurosci 8, P126 (2007) doi:10.1186/1471-2202-8-S2-P126

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Keywords

  • Firing Rate
  • Lateral Inhibition
  • Patch Clamp Recording
  • Mitral Cell
  • Odor Discrimination