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Inhalation frequency controls reformatting of mitral/tufted cell odor representations in the olfactory bulb

Marta Díaz-Quesada, Isaac A. Youngstrom, Yusuke Tsuno, Kyle R. Hansen, Michael N. Economo, Matt Wachowiak
doi: https://doi.org/10.1101/242784
Marta Díaz-Quesada
1Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, UT 84112
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Isaac A. Youngstrom
1Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, UT 84112
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Yusuke Tsuno
1Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, UT 84112
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Kyle R. Hansen
2Department of Bioengineering, University of Utah, Salt Lake city, UT 84112
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Michael N. Economo
1Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, UT 84112
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Matt Wachowiak
1Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, UT 84112
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Abstract

In mammals olfactory sensation depends on inhalation, which controls activation of sensory neurons and temporal patterning of central activity. Odor representations by mitral and tufted (MT) cells, the main output from the olfactory bulb (OB), reflect sensory input as well as excitation and inhibition from OB circuits, which may change as sniff frequency increases. To test the impact of sampling frequency on MT cell odor responses, we obtained whole-cell recordings from MT cells in anesthetized male and female mice while varying inhalation frequency via tracheotomy, allowing comparison of inhalation-linked responses across cells. We characterized frequency effects on MT cell responses during inhalation of air and odorants using inhalation pulses and also ‘playback’ of sniffing recorded from awake mice. Inhalation-linked changes in membrane potential were well-predicted across frequency from linear convolution of 1 Hz responses and, as frequency increased, near-identical temporal responses could emerge from depolarizing, hyperpolarizing or multiphasic MT responses. However, net excitation was not well predicted from 1 Hz responses and varied substantially across MT cells, with some cells increasing and others decreasing in spike rate. As a result, sustained odorant sampling at higher frequencies led to increasing decorrelation of the MT cell population response pattern over time. Bulk activation of sensory inputs by optogenetic stimulation affected MT cells more uniformly across frequency, suggesting that frequency-dependent decorrelation emerges from odor-specific patterns of activity in the OB network. These results suggest that sampling behavior alone can reformat early sensory representations, possibly to optimize sensory perception during repeated sampling.

Significance statement Olfactory sensation in mammals depends on inhalation, which increases in frequency during active sampling of olfactory stimuli. We asked how inhalation frequency can shape the neural coding of odor information by recording from projection neurons of the olfactory bulb while artificially varying odor sampling frequency in the anesthetized mouse. We found that sampling an odor at higher frequencies led to diverse changes in net responsiveness, as measured by action potential output, that were not predicted from low-frequency responses. These changes led to a reorganization of the pattern of neural activity evoked by a given odorant that occurred preferentially during sustained, high-frequency inhalation. These results point to a novel mechanism for modulating early sensory representations solely as a function of sampling behavior.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 04, 2018.
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Inhalation frequency controls reformatting of mitral/tufted cell odor representations in the olfactory bulb
Marta Díaz-Quesada, Isaac A. Youngstrom, Yusuke Tsuno, Kyle R. Hansen, Michael N. Economo, Matt Wachowiak
bioRxiv 242784; doi: https://doi.org/10.1101/242784
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Inhalation frequency controls reformatting of mitral/tufted cell odor representations in the olfactory bulb
Marta Díaz-Quesada, Isaac A. Youngstrom, Yusuke Tsuno, Kyle R. Hansen, Michael N. Economo, Matt Wachowiak
bioRxiv 242784; doi: https://doi.org/10.1101/242784

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