Key points GABAergic periglomerular (PG) cells in the olfactory bulb are proposed to mediate a “high-pass” filter at a single glomerulus that selectively blocks weak stimulus signals. Their efficacy may reflect their intrinsically small size and high input resistance, which allows them to be easily excited. We found that PG cells were in fact no more likely to be activated by weak stimuli than excitatory neurons. PG cells fired action potentials more readily in response to a fixed current input, but this advantage for excitability was offset by small synaptic currents. Glomeruli nevertheless display an excitation/inhibition balance that can support a high pass filter, shifting from unfavorable to favorable with increasing stimulus strength. Factors shaping the filter include glial glutamate transporters and presynaptic metabotropic glutamate receptors. We conclude that a single glomerulus may act as a high-pass filter to enhance stimulus contrast through mechanisms that are largely independent of cell-intrinsic properties. Abstract

GABAergic periglomerular (PG) cells in the olfactory bulb are proposed to mediate an intraglomerular “high-pass” filter through inhibition targeted onto a glomerulus. With this mechanism, weak stimuli (e.g., an odor with a low affinity for an odorant receptor) mainly produce PG cell-driven inhibition but strong stimuli generate enough excitation to overcome inhibition. PG cells may be particularly susceptible to being activated by weak stimuli due to their intrinsically small size and high input resistance. Here, we used dual-cell patch-clamp recordings and imaging methods in bulb slices obtained from wild-type and transgenic rats with labeled GABAergic cells to test a number of predictions of the high-pass filtering model. We first directly compared the responsiveness of PG cells with that of external tufted cells (eTCs), which are a class of excitatory cells that reside in a parallel but opposing position in the glomerular circuitry. PG cells were in fact found to be no more responsive than eTCs at low levels of sensory neuron activity. While PG cells required smaller currents to be excited, this advantage was offset by the fact that a given level of sensory neuron activity produced much smaller synaptic currents. We did however identify other factors that shaped the excitation/inhibition balance in a manner that would support a high-pass filter, including glial glutamate transporters and presynaptic metabotropic glutamate receptors. We conclude that a single glomerulus may act as a high-pass filter to enhance the contrast between different olfactory stimuli through mechanisms that are largely independent cell-intrinsic properties.

Abstract figure legend Mechanisms underlying a high-pass filter in olfactory bulb glomeruli.

A, Conceptual illustration of the intraglomerular high-pass filter model for olfactory information processing tested by this study. Weak olfactory sensory neuron (OSN) activity (left) results in an unfavorable excitation/inhibition (E/I) balance in a glomerulus (Glom) and block of output, while strong OSN activity (right) produces enough excitation to overcome inhibition. The differential responsiveness could facilitate discrimination of different odors that activate an odorant receptor to different degrees. B, Circuitry of a glomerulus. This study examined the relative effectiveness of different OSN activity levels in exciting glutamatergic external tufted cells (eTCs) and GABAergic periglomerular (PG) cells. eTCs and PG cells reside in key intermediate positions within the circuitry of the bulb, impacting the excitation/inhibition balance in mitral cells (MCs). C, Images of different Alexa-488-labeled PG cells and eTCs that were used in the electrophysiological and calcium imaging analyses.

This article is protected by copyright. All rights reserved