Differences in Glomerular-Layer-Mediated Feedforward Inhibition onto Mitral and Tufted Cells Lead to Distinct Modes of Intensity Coding

Abstract

Understanding how each of the many interneuron subtypes affects brain network activity is critical. In the mouse olfactory system, mitral cells (MCs) and tufted cells (TCs) comprise parallel pathways of olfactory bulb output that are thought to play distinct functional roles in odor coding. Here, in acute mouse olfactory bulb slices, we test how the two major classes of olfactory bulb interneurons differentially contribute to differences in MC versus TC response properties. We show that, whereas TCs respond to olfactory sensory neuron (OSN) stimulation with short latencies regardless of stimulation intensity, MC latencies correlate negatively with stimulation intensity. These differences between MCs and TCs are caused in part by weaker excitatory and stronger inhibitory currents onto MCs than onto TCs. These differences in inhibition between MCs and TCs are most pronounced during the first 150 ms after stimulation and are mediated by glomerular layer circuits. Therefore, blocking inhibition originating in the glomerular layer, but not granule-cell-mediated inhibition, reduces MC spike latency at weak stimulation intensities and distinct temporal patterns of odor-evoked responses in MCs and TCs emerge in part due to differences in glomerular-layer-mediated inhibition.

Basal forebrain GABAergic innervation of olfactory bulb periglomerular interneurons

“…) but match well with the prolonged ON‐evoked firing in mitral and tufted cells (Najac et al . ; Geramita & Urban, ). Moreover, 17/18 cells in this group responded to the photo stimulation of the basal forebrain axons with a prolonged IPSC (IPSC amplitude 193 ± 247 pA, range 11–850 pA; average decay time constant 116 ± 63 ms, range 40–254 ms, P < 0.0001 for comparison with both CR‐like and CB‐like PG cells, Wilcoxon test) (Fig.…”

Complex neural representation of odour information in the olfactory bulb

“…Therefore, TCs are presumably more efficient at distinguishing similar odorants at low concentration . These functional differences between MCs and TCs are likely because of the different inhibitory effects from the glomerular layer and granule cell layer . In addition, MCs and TCs project their axons to many non‐overlapping regions: axonal projections of TCs are restricted to the rostral structures, while MCs cover entire olfactory cortex uniformly and extend to caudal regions (Figure B) .…”

“…Temporal coding, however, focuses on the timing properties of M/T cell firing in response to odours. The latency to the first spike, the firing pattern and local field potential (LFP) theta oscillations across a short time window such as a sniff, and the overall firing pattern from M/T ensembles are all critical for representation of odour identity and intensity . The temporal coding strategy is supported by evidence from electrophysiological recordings in both anaesthetized and awake rodents …”

Interneuron functional diversity in the mouse accessory olfactory bulb

“…The MOB has several interneuron types, collectively termed JGCs, which reside in and around the glomerular layer (Larriva-Sahd, 2008;Yokosuka, 2012). In the MOB, JGCs include excitatory external tufted cells, several types of inhibitory periglomerular cells, and short axon cells (Shipley and Ennis, 1996;Schoppa et al, 1998;Aungst et al, 2003;Parrish-Aungst et al, 2007;Shao et al, 2009;Liu et al, 2013;Najac et al, 2015;Burton et al, 2017;Geramita and Urban, 2017). In the AOB, very few electrophysiological inquiries have been undertaken on JGCs (Goldmakher and Moss, 2000;Hu et al, 2016).…”