Smell

The world is undergoing massive atmospheric and ecological change, driving unprecedented challenges to human well-being. Olfaction is a key sensory system through which these impacts occur. The sense of smell influences quality of and satisfaction with life, emotion, emotion regulation, cognitive function, social interactions, dietary choices, stress, and depressive symptoms. Exposures via the olfactory pathway can also lead to (anti-)inflammatory outcomes. Increased understanding is needed regarding the ways in which odorants generated by nature (i.e., natural olfactory environments) affect human well-being. With perspectives from a range of health, social, and natural sciences, we provide an overview of this unique sensory system, four consensus statements regarding olfaction and the environment, and a conceptual framework that integrates the olfactory pathway into an understanding of the effects of natural environments on human well-being. We then discuss how this framework can contribute to better accounting of the impacts of policy and land-use decision-making on natural olfactory environments and, in turn, on planetary health.

Historically, the human sense of smell has been regarded as the odd stepchild of the senses, especially compared to the sensory bravado of seeing, touching, and hearing. The idea that the human olfaction has little to contribute to our experience of the world is commonplace, though with the emergence of COVID-19 there has rather been a sea change in this understanding. An ever increasing body of work has convincingly highlighted the keen capabilities of the human nose and the sophistication of the human olfactory system. Here, we provide a concise overview of the neuroscience of human olfaction spanning the last 10-15 years, with focus on the peripheral and central mechanisms that underlie how odor information is processed, packaged, parceled, predicted, and perturbed to serve odor-guided behaviors. We conclude by offering some guideposts for harnessing the next decade of olfactory research in all its shapes and forms.

Animals have evolved to rapidly detect and recognize brief and intermittent encounters with odor packages, exhibiting recognition capabilities within milliseconds. Artificial olfaction has faced challenges in achieving comparable results-existing solutions are either slow; or bulky, expensive, and power-intensive-limiting applicability in real-world scenarios for mobile robotics. Here, we introduce a miniaturized high-speed electronic nose, characterized by high-bandwidth sensor readouts, tightly controlled sensing parameters, and powerful algorithms. The system is evaluated on a high-fidelity odor delivery benchmark. We showcase successful classification of tens-of-millisecond odor pulses and demonstrate temporal pattern encoding of stimuli switching with up to 60 hertz. Those timescales are unprecedented in miniaturized low-power settings and demonstrably exceed the performance observed in mice. It is now possible to match the temporal resolution of animal olfaction in robotic systems. This will allow for addressing challenges in environmental and industrial monitoring, security, neuroscience, and beyond.

Animals exhibit innate behaviors that are stereotyped responses to specific evolutionarily relevant stimuli in the absence of prior learning or experience. The posterolateral cortical amygdala (plCoA) mediates innate attraction and aversion to odor. Here, we sought to define the circuit features of plCoA that give rise to innate attraction and aversion to odor in mice. First, we examined odor-evoked responses in these areas and found sparse encoding of odor identity, but not valence. We next considered a topographic organization and found that optogenetic stimulation of the anterior and posterior domains of plCoA elicits avoidance and attraction, respectively, suggesting a functional axis for valence. Using single-cell and spatial RNA sequencing, we identified the molecular cell types in plCoA, revealing an anteroposterior gradient in glutamatergic neurons that are sufficient and partially necessary for behavior. Finally, we identified topographically organized projections, whereby anterior neurons preferentially project to medial amygdala, and posterior neurons preferentially project to nucleus accumbens, which are respectively sufficient and necessary for innate attraction and aversion. Together, these data support a model whereby distinct, topographically distributed plCoA populations direct innate olfactory responses by signaling to divergent valence-specific targets, linking upstream olfactory identity to downstream valence behaviors, through a population code.