From chemotaxis to the cognitive map: the function of olfaction

Abstract

A paradox of vertebrate brain evolution is the unexplained variability in the size of the olfactory bulb (OB), in contrast to other brain regions, which scale predictably with brain size. Such variability appears to be the result of selection for olfactory function, yet there is no obvious concordance that would predict the causal relationship between OB size and behavior. This discordance may derive from assuming the primary function of olfaction is odorant discrimination and acuity. If instead the primary function of olfaction is navigation, i.e., predicting odorant distributions in time and space, variability in absolute OB size could be ascribed and explained by variability in navigational demand. This olfactory spatial hypothesis offers a single functional explanation to account for patterns of olfactory system scaling in vertebrates, the primacy of olfaction in spatial navigation, even in visual specialists, and proposes an evolutionary scenario to account for the convergence in olfactory structure and function across protostomes and deuterostomes. In addition, the unique percepts of olfaction may organize odorant information in a parallel map structure. This could have served as a scaffold for the evolution of the parallel map structure of the mammalian hippocampus, and possibly the arthropod mushroom body, and offers an explanation for similar flexible spatial navigation strategies in arthropods and vertebrates.

Fig. 1.

Schematic predictions of the spatial olfaction hypothesis. A hypothetical orthogonal grid created by plumes from two odorants, A and B, which increase in concentration from one to three arbitrary units. With increasing intensity, there is a qualitative shift in percept (indicated by color). This further divides the hypothetical olfactory space into subregions known as neighborhoods (see text).

Fig. 2.

Schematic predictions of the spatial olfaction hypothesis. The distribution of synthetic odor objects are landmarks in a dynamic olfactory space. (A) Encoding of odorant ratios as synthetic odor object percepts. (B) Synthetic objects occur at known locations, as defined by odorant ratios, and therefore are landmarks in olfactory space. (C) The coordinate of a synthetic object can therefore be computed from its elemental components. The coordinate system variables (u, v) are adopted from meteorology, where u designates streamwise direction and v crosswind direction (38).

Fig. 3.

The parallel map theory of navigation, illustrated with real-world examples and with abstract schematics. (A) BE: colored arrows indicate the vector information extracted from two directional cues, a distant mountain (yellow) and the polarized shape of an oblong body of water (blue). The schematic shows the abstract bicoordinate map and movements of a navigator. (B) SKs: colored shapes outline three unique positional cues. The schematic represents three SKs near the home base of the navigator, with each SK differing not in the number or characteristics of the cues but in the topology of the array. (C) Integrated map: by encoding the location of positional cues (i.e., SKs) on a bicoordinate map (i.e., BE), the navigator can compute novel vectors between two known points, i.e., cognitively map.