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Olfactory input is critical for sustaining odor quality codes in human orbitofrontal cortex

Abstract

Ongoing sensory input is critical for shaping internal representations of the external world. Conversely, a lack of sensory input can profoundly perturb the formation of these representations. The olfactory system is particularly vulnerable to sensory deprivation, owing to the widespread prevalence of allergic, viral and chronic rhinosinusitis, but how the brain encodes and maintains odor information under such circumstances remains poorly understood. Here we combined functional magnetic resonance imaging (fMRI) with multivariate (pattern-based) analyses and psychophysical approaches to show that a 7-d period of olfactory deprivation induces reversible changes in odor-evoked fMRI activity in piriform cortex and orbitofrontal cortex (OFC). Notably, multivoxel ensemble codes of odor quality in OFC became decorrelated after deprivation, and the magnitude of these changes predicted subsequent olfactory perceptual plasticity. Our findings suggest that transient changes in these key olfactory brain regions are instrumental in sustaining odor perception integrity in the wake of disrupted sensory input.

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Figure 1: Experimental design.
Figure 2: Rhinological data and nasal endoscopic measurements.
Figure 3: fMRI experiment 1: univariate fMRI results.
Figure 4: fMRI experiment 2: behavioral and multivariate fMRI results.
Figure 5: General deprivation-related changes in fMRI ensemble activity (fMRI experiment 2).

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Acknowledgements

The authors would like to thank M. Cahill for assistance in nasal endoscopy and acoustic rhinometry measurements, N. Sandalow and K. Phillips for technical assistance and data collection, and S. Warrenburg (International Flavors and Fragrances) for providing the odorless grade solvents. This work was supported by Northwestern Institutional Predoctoral Training Awards to K.N.W. (T32NS047987) and to J.D.H. (2T32 MH067564), grants R01DC010014 and K08DC007653 from the US National Institute on Deafness and Other Communication Disorders to J.A.G., and US National Institutes of Health grant M01-RR00048 from the National Center for Research Resources to Northwestern University Feinberg School of Medicine.

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J.A.G. conceived the experiment, with extensive contributions and methodological suggestions from K.N.W., D.B.C. and J.D.H. K.N.W. collected the imaging and behavioral data. D.B.C. and B.K.T. collected and analyzed the nasal endoscopy and rhinometry data. K.N.W. analyzed the behavioral and imaging data with assistance from J.D.H. and J.A.G. K.N.W., J.D.H. and J.A.G. wrote the manuscript.

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Correspondence to Keng Nei Wu or Jay A Gottfried.

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The authors declare no competing financial interests.

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Wu, K., Tan, B., Howard, J. et al. Olfactory input is critical for sustaining odor quality codes in human orbitofrontal cortex. Nat Neurosci 15, 1313–1319 (2012). https://doi.org/10.1038/nn.3186

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