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

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

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.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adolescent
  • Adult
  • Entorhinal Cortex / diagnostic imaging*
  • Entorhinal Cortex / physiology
  • Female
  • Functional Neuroimaging
  • Grid Cells / physiology*
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Neural Pathways / diagnostic imaging
  • Neural Pathways / physiology
  • Olfactory Perception / physiology*
  • Prefrontal Cortex / diagnostic imaging*
  • Prefrontal Cortex / physiology
  • Spatial Navigation / physiology*
  • Young Adult