Abstract

The organization of representations in the brain has been observed to locally reflect subspaces of inputs that are relevant to behavioral or perceptual feature combinations, such as in areas receptive to lower and higher-order features in the visual system. The early olfactory system developed highly plastic mechanisms and convergent evidence indicates that projections from primary neurons converge onto the glomerular level of the olfactory bulb (OB) to form a code composed of continuous spatial zones that are differentially active for particular physico-chemical feature combinations, some of which are known to trigger behavioral responses. In a model study of the early human olfactory system, we derive a glomerular organization based on a set of real-world, biologically relevant stimuli, a distribution of receptors that respond each to a set of odorants of similar ranges of molecular properties, and a mechanism of axon guidance based on activity. Apart from demonstrating activity-dependent glomeruli formation and reproducing the relationship of glomerular recruitment with concentration, it is shown that glomerular responses reflect similarities of human odor category perceptions and that further, a spatial code provides a better correlation than a distributed population code. These results are consistent with evidence of functional compartmentalization in the OB and could suggest a function for the bulb in encoding of perceptual dimensions.

Highlights

  • Complex repertoires of olfactory receptors (OR) evolved in different numbers over species

  • We reduced the resulting matrix by multi-dimensional scaling (MDS) to three dimensions and obtained coordinate points corresponding to each olfactory axon bundle

  • Subfigure (C) is an illustration of how olfactory axons project from epithelium to glomeruli in a small network consisting of five OR types and five ORNs per type

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Summary

Introduction

Complex repertoires of olfactory receptors (OR) evolved in different numbers over species. The OB is a crucial processing station for olfactory signals (Buschhüter et al, 2008) and glomeruli are thought to be functional units and convergence target for axons from many ORNs of just one type of odorant receptor (OR) (Kauer and Cinelli, 1993; Mori, 1999; Bozza et al, 2002; Mombaerts, 2004), so that each odorant elicits a specific map of glomerular activation (e.g., Ressler et al, 1994). It is known that ORN type-convergence onto glomeruli is at least partly mediated by experience (Yu et al, 2004; Kerr and Belluscio, 2006; Imai and Sakano, 2007) and that activity plays a role in axon fate (Ming et al, 2002; Mombaerts, 2006; Sakano, 2010; Mori and Sakano, 2011). Direction of the axon’s growth cone is regulated by various chemical cues, diffusible chemoattractants, and repellants, in a series of discrete steps (Sanes and Jessell, 2000). Serizawa et al (2006) found evidence in the mouse that correlation of neural activity mediated axonal attraction and repulsion by up- and down-regulation of a set of olfactory axon guidance cues, which suggested that axon sorting could be based on correlated neural activity

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