Spatial information from the odour environment in mammalian olfaction

Abstract

The sense of smell is an essential modality for many species, in particular nocturnal and crepuscular mammals, to gather information about their environment. Olfactory cues provide information over a large range of distances, allowing behaviours ranging from simple detection and recognition of objects, to tracking trails and navigating using odour plumes from afar. In this review, we discuss the features of the natural olfactory environment and provide a brief overview of how odour information can be sampled and might be represented and processed by the mammalian olfactory system. Finally, we discuss recent behavioural approaches that address how mammals extract spatial information from the environment in three different contexts: odour trail tracking, odour plume tracking and, more general, olfactory-guided navigation. Recent technological developments have seen the spatiotemporal aspect of mammalian olfaction gain significant attention, and we discuss both the promising aspects of rapidly developing paradigms and stimulus control technologies as well as their limitations. We conclude that, while still in its beginnings, research on the odour environment offers an entry point into understanding the mechanisms how mammals extract information about space.

How the evolution of air breathing shaped hippocampal function

“…Studies of the neural basis of spatial olfaction in murines and humans are emerging to support the thesis of the olfactory spatial hypothesis [19,56,60,61]. For example, in a recent summary of the field, Marin et al [19] proposed that the concept of odour spatial neighbourhoods could explain recent results of a grid-like pattern in human piriform cortex [62]. Also in humans, hippocampal activation and virtual maze performance correlates with olfactory discrimination accuracy [63].…”

“…Yet olfaction, a sensory modality that is both a phylogenetically conserved primary input to the hippocampus [10,11], and a primary sensory modality for murines [12,13], has rarely been studied in the context of spatial orientation in these species (but see [14][15][16][17]). This is slowly changing [18,19].…”

Active sensing in a dynamic olfactory world

“…Indeed, neurons in the AON pars externa are excited by ipsi-nostril and contra-nostril-only stimulation with odorants of similar quality during each respiratory cycle (Kikuta et al, 2010). Evidence is also accumulating that stereo-olfaction can contribute to odordriven navigation (Catania, 2013;Khan et al, 2012;Liu et al, 2020;Marin et al, 2021).…”

Principles of odor coding in vertebrates and artificial chemosensory systems

“…In open spaces, chemical cues (odorants) originate from point sources under the action of carriers, typically wind, and obstacles can elicit drifting turbulent odorant plumes (791). The concentration of odorants in plumes is highly variable in time and space (792).…”