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Neuron. 2019 Jun 5;102(5):1066-1075.e5. doi: 10.1016/j.neuron.2019.03.034. Epub 2019 Apr 22.

Grid-like Neural Representations Support Olfactory Navigation of a Two-Dimensional Odor Space.

Author information

1
Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA. Electronic address: xiaojunbao2011@u.northwestern.edu.
2
Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
3
Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA; Department of Psychology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, IL 60208, USA.
4
Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: jaygottf@pennmedicine.upenn.edu.

Abstract

Searching for food, friends, and mates often begins with an airborne scent. Importantly, odor concentration rises with physical proximity to an odorous source, suggesting a framework for orienting within olfactory landscapes to optimize behavior. Here, we created a two-dimensional odor space composed purely of odor stimuli to model how a navigator encounters smells in a natural environment. We show that human subjects can learn to navigate in olfactory space and form predictions of to-be-encountered smells. During navigation, fMRI responses in entorhinal cortex and ventromedial prefrontal cortex take the form of grid-like representations with hexagonal periodicity and entorhinal grid strength scaled with behavioral performance across subjects. The identification of olfactory grid-like codes with 6-fold symmetry highlights a unique neural mechanism by which odor information can be assembled into spatially navigable cognitive maps, optimizing orientation, and path finding toward an odor source.

KEYWORDS:

cognitive map; entorhinal cortex; fMRI; grid cells; human; odor coding; olfactory navigation; prefrontal cortex

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