Literature DB >> 33953395

Fast odour dynamics are encoded in the olfactory system and guide behaviour.

Tobias Ackels1,2, Andrew Erskine1,2, Debanjan Dasgupta1,2, Alina Cristina Marin1, Tom P A Warner1, Sina Tootoonian1,2, Izumi Fukunaga1, Julia J Harris1,2, Andreas T Schaefer3,4.   

Abstract

Odours are transported in turbulent plumes, which result in rapid concentration fluctuations1,2 that contain rich information about the olfactory scenery, such as the composition and location of an odour source2-4. However, it is unclear whether the mammalian olfactory system can use the underlying temporal structure to extract information about the environment. Here we show that ten-millisecond odour pulse patterns produce distinct responses in olfactory receptor neurons. In operant conditioning experiments, mice discriminated temporal correlations of rapidly fluctuating odours at frequencies of up to 40 Hz. In imaging and electrophysiological recordings, such correlation information could be readily extracted from the activity of mitral and tufted cells-the output neurons of the olfactory bulb. Furthermore, temporal correlation of odour concentrations5 reliably predicted whether odorants emerged from the same or different sources in naturalistic environments with complex airflow. Experiments in which mice were trained on such tasks and probed using synthetic correlated stimuli at different frequencies suggest that mice can use the temporal structure of odours to extract information about space. Thus, the mammalian olfactory system has access to unexpectedly fast temporal features in odour stimuli. This endows animals with the capacity to overcome key behavioural challenges such as odour source separation5, figure-ground segregation6 and odour localization7 by extracting information about space from temporal odour dynamics.

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Year:  2021        PMID: 33953395      PMCID: PMC7611658          DOI: 10.1038/s41586-021-03514-2

Source DB:  PubMed          Journal:  Nature        ISSN: 0028-0836            Impact factor:   49.962


  38 in total

Review 1.  Mechanisms of animal navigation in odor plumes.

Authors:  N J Vickers
Journal:  Biol Bull       Date:  2000-04       Impact factor: 1.818

Review 2.  The sniff as a unit of olfactory processing.

Authors:  Adam Kepecs; Naoshige Uchida; Zachary F Mainen
Journal:  Chem Senses       Date:  2005-12-08       Impact factor: 3.160

3.  'Infotaxis' as a strategy for searching without gradients.

Authors:  Massimo Vergassola; Emmanuel Villermaux; Boris I Shraiman
Journal:  Nature       Date:  2007-01-25       Impact factor: 49.962

4.  Olfactory computation and object perception.

Authors:  J J Hopfield
Journal:  Proc Natl Acad Sci U S A       Date:  1991-08-01       Impact factor: 11.205

5.  Precise olfactory responses tile the sniff cycle.

Authors:  Roman Shusterman; Matthew C Smear; Alexei A Koulakov; Dmitry Rinberg
Journal:  Nat Neurosci       Date:  2011-07-17       Impact factor: 24.884

6.  High-speed odor transduction and pulse tracking by insect olfactory receptor neurons.

Authors:  Paul Szyszka; Richard C Gerkin; C Giovanni Galizia; Brian H Smith
Journal:  Proc Natl Acad Sci U S A       Date:  2014-11-10       Impact factor: 11.205

7.  Sensory biology. Flower discrimination by pollinators in a dynamic chemical environment.

Authors:  Jeffrey A Riffell; Eli Shlizerman; Elischa Sanders; Leif Abrell; Billie Medina; Armin J Hinterwirth; J Nathan Kutz
Journal:  Science       Date:  2014-06-27       Impact factor: 47.728

8.  Spatial Information in the Three-Dimensional Fine Structure of an Aquatic Odor Plume.

Authors:  P A Moore; J Atema
Journal:  Biol Bull       Date:  1991-12       Impact factor: 1.818

9.  The speed of smell: odor-object segregation within milliseconds.

Authors:  Paul Szyszka; Jacob S Stierle; Stephanie Biergans; C Giovanni Galizia
Journal:  PLoS One       Date:  2012-04-27       Impact factor: 3.240

10.  An olfactory cocktail party: figure-ground segregation of odorants in rodents.

Authors:  Dan Rokni; Vivian Hemmelder; Vikrant Kapoor; Venkatesh N Murthy
Journal:  Nat Neurosci       Date:  2014-08-03       Impact factor: 24.884

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  12 in total

1.  State-dependent representations of mixtures by the olfactory bulb.

Authors:  Aliya Mari Adefuin; Sander Lindeman; Janine Kristin Reinert; Izumi Fukunaga
Journal:  Elife       Date:  2022-03-07       Impact factor: 8.140

2.  Active sensing in a dynamic olfactory world.

Authors:  John Crimaldi; Hong Lei; Andreas Schaefer; Michael Schmuker; Brian H Smith; Aaron C True; Justus V Verhagen; Jonathan D Victor
Journal:  J Comput Neurosci       Date:  2021-09-30       Impact factor: 1.621

Review 3.  The structures and functions of correlations in neural population codes.

Authors:  Stefano Panzeri; Monica Moroni; Houman Safaai; Christopher D Harvey
Journal:  Nat Rev Neurosci       Date:  2022-06-22       Impact factor: 38.755

4.  Learning to predict target location with turbulent odor plumes.

Authors:  Nicola Rigolli; Nicodemo Magnoli; Lorenzo Rosasco; Agnese Seminara
Journal:  Elife       Date:  2022-08-12       Impact factor: 8.713

5.  Sample Preparation and Warping Accuracy for Correlative Multimodal Imaging in the Mouse Olfactory Bulb Using 2-Photon, Synchrotron X-Ray and Volume Electron Microscopy.

Authors:  Yuxin Zhang; Tobias Ackels; Alexandra Pacureanu; Marie-Christine Zdora; Anne Bonnin; Andreas T Schaefer; Carles Bosch
Journal:  Front Cell Dev Biol       Date:  2022-06-08

Review 6.  Transgenic mice encoding modern imaging probes: Properties and applications.

Authors:  Ludmila A Kasatkina; Vladislav V Verkhusha
Journal:  Cell Rep       Date:  2022-05-24       Impact factor: 9.995

7.  Getting out the caliper: Behavioral quantification of perceptual odor similarity.

Authors:  Tobias Ackels; Andreas T Schaefer
Journal:  Cell Rep Methods       Date:  2022-06-20

8.  Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes.

Authors:  Viraaj Jayaram; Nirag Kadakia; Thierry Emonet
Journal:  Elife       Date:  2022-01-24       Impact factor: 8.140

Review 9.  Processing of Odor Information During the Respiratory Cycle in Mice.

Authors:  Kensaku Mori; Hitoshi Sakano
Journal:  Front Neural Circuits       Date:  2022-03-31       Impact factor: 3.492

10.  Sparse connectivity for MAP inference in linear models using sister mitral cells.

Authors:  Sina Tootoonian; Andreas T Schaefer; Peter E Latham
Journal:  PLoS Comput Biol       Date:  2022-01-31       Impact factor: 4.475

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