Most animals rely greatly on their sense of smell in sniffing out familiar and unfamiliar habitats. As they search for food, follow their mates, and forage, they often are able to recall their previous hunting locations by smell with incredible success and high spatial resolution. Despite this obvious significance of smell to animal behavior, it has been remarkably understudied. The underlying cause links to anthropocentric chauvinism. Olfaction did not garner greater scientific interest because it appeared less pertinent to understanding human cognition, and the human sense of smell was disregarded for centuries because it was believed to be inferior to that of other animals and less noteworthy behaviorally. Nothing could be further from the truth, however. The human sense of smell is significantly more sophisticated than its generally poor reputation indicates. Meanwhile, this error in judgment is being re-evaluated and, gradually, corrected (Shepherd, 2004). Research conducted on smell over the past decades has uncovered new modeling possibilities and provided several reasons to re-evaluate our assumptions about how the brain functions.

How the brain encodes and stores information acquired from the distal stimulus is a major topic of study in olfaction. Essentially, there are two critical parts to this inquiry. Firstly, we still don't know how the brain represents odors, meaning how neural space is functionally allocated to group qualitative and physicochemical characteristics of the chemical stimulus. Notably, the olfactory cortex differs from the visual and auditory sensory cortices in that it does not have a stereotypical and topographical ordering of the sensory input it receives (Barwich, 2020). The latest research has even provided evidence for the presence of representational drift in the piriform cortex in response to the olfactory stimulus. Within a month, neuronal populations fundamentally change how they distribute their activity in response to an odor (Schoonover et al., 2021). Such findings lend further support to the progressively attractive idea that non-topographic encoding is critical to how the olfactory system operates. To be sure, the wider theoretical implications of such non-topographic encoding of olfactory information are still debated and may assist future research on other sensory cortices in their linkage to cognitive and motor activities. Secondly, more research is especially needed investigating the use of smell by animals in navigating and remembering definite locations in their environment.

How does the brain associate smell with different places (or vice versa)? Paradoxically, non-spatial odor encoding may hold the key to answering this question. The absence of a stable stimulus map in the piriform is possibly linked with an animal’s flexible navigational behavior towards a spatially fluctuating and promiscuous olfactory stimulus in the environment. When you consider the nature of the olfactory input in its contextual appearance – especially its unpredictable and contingent spatial distribution – the absence of topographic encoding makes sense from an ecological standpoint when observing a moving animal. (In addition, non-topography may be beneficial with respect to an odor's ambiguous and contextual meaning. Odorants can have varying behavioral importance for an animal based on their environmental context, as the same odorant can originate from different sources.)

Because volatile molecules are prone to airflow turbulence, any targeted mapping of the spatial distribution of odors in neural space is ecologically infeasible, if not a waste of resources. Despite this, we still face the scientific puzzle of how the brain can associate odors with specific locations, as humans and other animals frequently form strong associations between particular locations and scents.

Recent research by Poo et al. (2022) offers a possible explanation, paving the way for subsequent analysis and modeling. They explored how rats use odors to memorize behaviorally relevant locations and the structure of their surroundings, further shedding light on the mechanisms through which the brain combines spatial information with olfactory input. Specifically, Poo et al. focused on activity in the piriform, the most significant cortical region of the olfactory system, and whether or how it encodes spatial information. Their findings revealed that neurons in the piriform contribute to spatial cognition by generating joint representations for olfactory and spatial information.

Poo et al. (2022) trained six rats for roughly 6 weeks to navigate a raised, custom-made platform in the shape of a cross that pointed to four different locations. An odor was paired with a maze location, such that North, South, West, and East were each associated with distinct odorants. Rats sniffed the (randomly dispensed) scents at the trial's start port before deciding which of the four possible maze ports to poke. When the rats correctly connected an odor with a location port, they were rewarded. Each of the six rats underwent approximately 200 behavioral analysis trials, with a 70% success rate.

Complementing the behavioral analysis, three of the six rats were implanted with multielectrode drives to record neural activity during the trials. Single-cell analysis was used to derive conclusions regarding the similarities and differences between the CA1 region of the hippocampus and the posterior region of the piriform (pPCX). Recordings in the piriform revealed various activity patterns: some pPCX neurons responded only to odor identity, whereas others responded to odor identity and port location. Interestingly, a bigger percentage of pPCX neurons responded to location than identity (40% vs. 29%).

What do these outcomes suggest? The functional promiscuity of the piriform is potentially the main finding of the smell-space maze experiment. Instead of requiring two functionally different modalities and neural locations to express information about odor and place, olfactory processing can contain and further co-represent spatial information. While not all olfactory behavior is spatial or needs to contain spatial information, the findings of Poo et al. suggest that olfactory processing is functionally spatial in terms of integrating and co-processing spatial with olfactory information.

Frankly, that is already a big deal. It opens two conceptual directions. First, this co-representation of olfactory and spatial representation in piriform provides further support for the inherently contextual encoding of environmental information, as opposed to the localist notion of modality-specific allocations of sensory information to functionally distinct neural domains. Connected to other findings regarding the piriform cortex as target-driven but non-input structured, the piriform appears to be less committed to stable odor representation than it is to coupling odor information with behaviorally given information such as spatial location.

Second, when we consider how animals use odors for navigation outside the laboratory, another perspective emerges. The animals in Poo et al. were trained to navigate a fixed reference frame in which scents were correlated with stable but arbitrarily assigned locations. Now contrast this with a more ecologically realistic context in which an animal must seek or relocate possibly mobile sources of indeterminate distance. In other words, while we have a finding of spatial information encoding in piriform, how animals use (fluctuating) olfactory information to navigate their environment remains to be understood. Another promising area for future research is memory storage of behaviorally more meaningful smell-space associations, particularly in light of representational drift to pure odor stimulation.

This brings us to conclude with a more philosophical and speculative note about Marcel Proust. Proust's autobiographical story about the madeleine (in Remembrance of Things Past) is intertwined with popular imagination about the relationship between smell and the recall of places and people. Contrary to popularized accounts, however, Proust does not specify or describe distinct odors in his madeleine episode. Instead, Proust's memories appear to be firmly linked to his repeated dipping of the madeleine into the tea. It would seem that the motor action is what really connects his perceptual sensations with his thoughts and memories.

From this perspective, it appears that scents are ideally adapted to serve as recall tags for an animal's autobiographical experience. Odors can function as sensory bridges to distinct behaviorally defined representations of an experience. Even though an olfactory encounter is always about something concrete in the present (i.e., a physically present stimulus), it often is not only about the current stimulus. This is a critical indicator of the wider behavioral function and neural representation of odors: odorants can have various attractor states linked to behavior (Skarda & Freeman, 1987). Understanding olfaction must therefore focus on how sensory signals are represented when they acquire behavioral meaning for an animal in its ecological niche.