Map Formation in the Olfactory Bulb by Axon Guidance of Olfactory Neurons

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.

Continuous spatial representations in the olfactory bulb may reflect perceptual categories

“…Experimental evidence and model studies point toward localized encoding also of behavioral or perceptual aspects in the rat (e.g., Dielenberg and McGregor, 2001; Linster et al, 2001; Kobayakawa et al, 2007; Raman and Gutierrez-Osuna, 2009; Sakano, 2010; Auffarth et al, 2011b). Furthermore, there could be an organizing principle of relative spatial locations of odorant representations, related to chemical similarity (Uchida et al, 2000; Cleland et al, 2002; Johnson et al, 2004), distribution of ORNs on the epithelium (rhinotopy; Miyamichi et al, 2005; Johnson and Leon, 2007), and behavioral relevance.…”

Understanding smell—The olfactory stimulus problem

“…By the simplest model, a measure of ligand similarity and stimulus correlation could serve as the basis for spatial arrangement (e.g. Auffarth et al, 2011c). By this model, odor perception is not the basis of spatial organization, but, on the contrary, would be expected to emerge based on natural stimulus statistics.…”

“…In rats, Auffarth et al (2011b) and Raman and Gutierrez-Osuna (2009) found indication that some odor categories can be predicted from spatially clustered areas of glomerular activity patterns and in a subsequent computational model, such a clustering was explained in part by structural similarities of odorants (Auffarth et al, 2011c). In the mice OB, Matsumoto et al (2010) found feature clusters that are associated with odorant categories and behavioral responses.…”

“…Haddad et al (2010) showed that the first principal component of activity at the level of the primary processing center in different animal species is highly correlated to approach or withdrawal in animals, or pleasantness in humans, which suggests that the primary processing center separates odors by a hedonic dimension. In several animal models and different levels of the system, there is evidence that perceptual features are related to the spatial topology Auffarth et al, 2011c;Matsumoto et al, 2010;Jefferis et al, 2007). In humans Lapid et al (2011) showed that spatial offsets on the receptor sheet are correlated with differences in pleasantness.…”

Chemosensory Learning and Memory

“…As Sandoz (2011) shows in his review, the honeybee has been a model for applying behavioral, neurophysiological and neuroanatomical techniques to research on olfactory learning. Two separate models of the role in olfactory learning of the rat olfactory bulb (Auffarth et al, 2011) and the human glomerulus (Schaefer and Margrie, 2012) are presented.…”