Differential Axonal Projection of Mitral and Tufted Cells in the Mouse Main Olfactory System

Abstract

In the past decade, much has been elucidated regarding the functional organization of the axonal connection of olfactory sensory neurons to olfactory bulb (OB) glomeruli. However, the manner in which projection neurons of the OB process odorant input and send this information to higher brain centers remains unclear. Here, we report long-range, large-scale tracing of the axonal projection patterns of OB neurons using two-photon microscopy. Tracer injection into a single glomerulus demonstrated widely distributed mitral/tufted cell axonal projections on the lateroventral surface of the mouse brain, including the anterior/posterior piriform cortex (PC) and olfactory tubercle (OT). We noted two distinct groups of labeled axons: PC-orienting axons and OT-orienting axons. Each group occupied distinct parts of the lateral olfactory tract. PC-orienting axons projected axon collaterals to a wide area of the PC but only a few collaterals to the OT. OT-orienting axons densely projected axon collaterals primarily to the anterolateral OT (alOT). Different colored dye injections into the superficial and deep portions of the OB external plexiform layer revealed that the PC-orienting axon populations originated in presumed mitral cells and the OT-orienting axons in presumed tufted cells. These data suggest that although mitral and tufted cells receive similar odor signals from a shared glomerulus, they process the odor information in different ways and send their output to different higher brain centers via the PC and alOT.

The Olfactory System

“…The relatively recent advent of approaches to visualize glomeruli in vivo combined with genetico-viral based tracing techniques, have made it feasible to address this question. The results of these studies have largely confirmed those implications from older tracing studies revealing, for example, that projections from sister MTCs of a single glomerulus, and those of a single cell, disperse to innervate multiple POC structures in a manner that is independent of the spatial location of an individual glomerulus (Nagayama et al, 2010;Ghosh et al, 2011;Miyamichi et al, 2011;Sosulski et al, 2011). Course topography is evident in some MOB targets as noted earlier for the AON (Miyamichi et al, 2011).…”

“…The caudal parts of piriform, periamygdaloid and lateral entorhinal cortices by contrast receive terminals primarily or exclusively from MCs. A recent study (Nagayama et al, 2010) confirmed older findings that TCs, compared to MCs, tend to project more strongly to rostral POC areas (e.g., olfactory tubercle, AON). Other results did not detect differences in the projections of deep or internal TCs compared to their sister MC cohorts (Ghosh et al, 2011).…”

“…TC axons, together with those of MCs, collateralize locally in the IPL/GCL on GCs then exit the MOB to innervate primary olfactory cortex (POC). There are differences in MC vs. TC projections to POC, with TCs projecting preferentially to the anterior olfactory nucleus, olfactory tubercle and rostral olfactory cortex (Nagayama et al, 2010;Igarashi et al, 2012).…”

Untypical connectivity from olfactory sensory neurons expressing OR37 into higher brain centers visualized by genetic tracing

“…Strotmann (&) Institute of Physiology, University of Hohenheim, Garbenstrasse 30, 70593 Stuttgart, Germany e-mail: strotman@uni-hohenheim.de glomeruli are currently unknown. By means of various labeling studies of the last decades, the general targets of projection neurons (mitral/tufted cells) from the main olfactory bulb (MOB) have been identiWed throughout the olfactory cortex, including the anterior olfactory nucleus, the piriform cortex and the entorhinal cortex (Haberly and Price 1977;Scott et al 1980;Luskin and Price 1982;Carlsen et al 1982;Ojima et al 1984;Buonviso et al 1991;Nagayama et al 2010;Miyamichi et al 2011;Ghosh et al 2011) as well as the cortical amygdala (Kevetter and Winans 1981b;Licht and Meredith 1987). In this context, it is interesting to note that in a recent study, Baum and coworkers have shown that an application of tracer in the ventral domain of the MOB resulted not only in the labeling of the typical target sites, but labeled Wbers were unexpectedly also found in the anterior and posterior subdivisions of the medial amygdala (Kang et al 2009).…”

Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling

“…The odour map in the OB is transmitted by output neurons, mitral cells, to higher olfactory centres and eventually translated to elicit appropriate behavioural and physiological responses. Recent anatomical studies in mice showed that axons from identified glomeruli project diffusely throughout the piriform cortex [6][7][8][9] , the largest target area of the OB, and that piriform neurons receive convergent inputs from multiple mitral cells distributed throughout the OB 10 . These findings are consistent with an optical imaging study that found no apparent spatial organization of odour-evoked activity patterns in the piriform cortex 11 .…”