Literature DB >> 30348674

Respiration Modulates Olfactory Memory Consolidation in Humans.

Artin Arshamian1,2,3,4, Behzad Iravani5, Asifa Majid2,3,6,7, Johan N Lundström5,8,9.   

Abstract

In mammals respiratory-locked hippocampal rhythms are implicated in the scaffolding and transfer of information between sensory and memory networks. These oscillations are entrained by nasal respiration and driven by the olfactory bulb. They then travel to the piriform cortex where they propagate further downstream to the hippocampus and modulate neural processes critical for memory formation. In humans, bypassing nasal airflow through mouth-breathing abolishes these rhythms and impacts encoding as well as recognition processes thereby reducing memory performance. It has been hypothesized that similar behavior should be observed for the consolidation process, the stage between encoding and recognition, were memory is reactivated and strengthened. However, direct evidence for such an effect is lacking in human and nonhuman animals. Here we tested this hypothesis by examining the effect of respiration on consolidation of episodic odor memory. In two separate sessions, female and male participants encoded odors followed by a 1 h awake resting consolidation phase where they either breathed solely through their nose or mouth. Immediately after the consolidation phase, memory for odors was tested. Recognition memory significantly increased during nasal respiration compared with mouth respiration during consolidation. These results provide the first evidence that respiration directly impacts consolidation of episodic events, and lends further support to the notion that core cognitive functions are modulated by the respiratory cycle.SIGNIFICANCE STATEMENT Memories pass through three main stages in their development: encoding, consolidation, and retrieval. Growing evidence from animal and human studies suggests that respiration plays an important role in the behavioral and neural mechanisms associated with encoding and recognition. Specifically nasal, but not mouth, respiration entrains neural oscillations that enhance encoding and recognition processes. We demonstrate that respiration also affects the consolidation stage. Breathing through the nose compared with the mouth during consolidation enhances recognition memory. This demonstrates, first, that nasal respiration is important during the critical period were memories are reactivated and strengthened. Second, it suggests that the neural mechanisms responsible may emerge from nasal respiration.
Copyright © 2018 the authors 0270-6474/18/3810286-09$15.00/0.

Entities:  

Keywords:  consolidation; episodic; hippocampus; memory; odor; respiration

Mesh:

Year:  2018        PMID: 30348674      PMCID: PMC6596216          DOI: 10.1523/JNEUROSCI.3360-17.2018

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  56 in total

1.  Functional magnetic resonance imaging (fMRI) activity in the hippocampal region during recognition memory.

Authors:  C E Stark; L R Squire
Journal:  J Neurosci       Date:  2000-10-15       Impact factor: 6.167

Review 2.  The sniff is part of the olfactory percept.

Authors:  Joel Mainland; Noam Sobel
Journal:  Chem Senses       Date:  2005-12-08       Impact factor: 3.160

3.  Olfactory reactions in the brain of the hedgehog.

Authors:  E D Adrian
Journal:  J Physiol       Date:  1942-03-31       Impact factor: 5.182

Review 4.  Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning.

Authors:  György Buzsáki
Journal:  Hippocampus       Date:  2015-10       Impact factor: 3.899

Review 5.  Olfactory system oscillations across phyla.

Authors:  Leslie M Kay
Journal:  Curr Opin Neurobiol       Date:  2014-10-24       Impact factor: 6.627

6.  The effect of mouth breathing on exercise induced fall in lung function in children with allergic asthma and rhinitis.

Authors:  Mirjana Turkalj; Jelena Živković; Marcel Lipej; Sandra Bulat Lokas; Damir Erceg; Srđan Ante Anzić; Robert Magdić; Davor Plavec
Journal:  Int J Pediatr Otorhinolaryngol       Date:  2016-04-19       Impact factor: 1.675

Review 7.  Olfactory oscillations: the what, how and what for.

Authors:  Leslie M Kay; Jennifer Beshel; Jorge Brea; Claire Martin; Daniel Rojas-Líbano; Nancy Kopell
Journal:  Trends Neurosci       Date:  2009-02-23       Impact factor: 13.837

8.  Long-term memory for odors: influences of familiarity and identification across 64 days.

Authors:  Stina Cornell Kärnekull; Fredrik U Jönsson; Johan Willander; Sverker Sikström; Maria Larsson
Journal:  Chem Senses       Date:  2015-03-04       Impact factor: 3.160

Review 9.  Breathing as a Fundamental Rhythm of Brain Function.

Authors:  Detlef H Heck; Samuel S McAfee; Yu Liu; Abbas Babajani-Feremi; Roozbeh Rezaie; Walter J Freeman; James W Wheless; Andrew C Papanicolaou; Miklós Ruszinkó; Yury Sokolov; Robert Kozma
Journal:  Front Neural Circuits       Date:  2017-01-12       Impact factor: 3.492

10.  From creation to consolidation: a novel framework for memory processing.

Authors:  Edwin M Robertson
Journal:  PLoS Biol       Date:  2009-01-27       Impact factor: 8.029

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  29 in total

1.  Blood pressure drives multispectral tuning of inspiration via a linked-loop neural network.

Authors:  Lauren S Segers; Sarah C Nuding; Mackenzie M Ott; Russell O'Connor; Kendall F Morris; Bruce G Lindsey
Journal:  J Neurophysiol       Date:  2020-09-23       Impact factor: 2.714

2.  The rhythm of memory: how breathing shapes memory function.

Authors:  Detlef H Heck; Robert Kozma; Leslie M Kay
Journal:  J Neurophysiol       Date:  2019-06-19       Impact factor: 2.714

Review 3.  Controlling neuronal assemblies: a fundamental function of respiration-related brain oscillations in neuronal networks.

Authors:  Shani Folschweiller; Jonas-Frederic Sauer
Journal:  Pflugers Arch       Date:  2022-05-31       Impact factor: 3.657

4.  The olfactory bulb coordinates the ventral hippocampus-medial prefrontal cortex circuit during spatial working memory performance.

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Journal:  J Physiol Sci       Date:  2022-04-25       Impact factor: 2.781

Review 5.  Inconclusive evidence that breathing shapes pupil dynamics in humans: a systematic review.

Authors:  Sylvia Edwards; Frans Nordén; Martin Schaefer; Johan N Lundström; Artin Arshamian
Journal:  Pflugers Arch       Date:  2022-07-25       Impact factor: 4.458

Review 6.  "The great mixing machine": multisensory integration and brain-breath coupling in the cerebral cortex.

Authors:  Detlef H Heck; Somogy Varga
Journal:  Pflugers Arch       Date:  2022-07-29       Impact factor: 4.458

7.  Temporal Relations between Cortical Network Oscillations and Breathing Frequency during REM Sleep.

Authors:  Adriano B L Tort; Maximilian Hammer; Jiaojiao Zhang; Jurij Brankačk; Andreas Draguhn
Journal:  J Neurosci       Date:  2021-05-07       Impact factor: 6.167

Review 8.  Ultrasonic Vocalizations Emission across Development in Rats: Coordination with Respiration and Impact on Brain Neural Dynamics.

Authors:  Julie Boulanger-Bertolus; Anne-Marie Mouly
Journal:  Brain Sci       Date:  2021-05-11

9.  Investigation on the Effect of Oral Breathing on Cognitive Activity Using Functional Brain Imaging.

Authors:  Ju-Yeon Jung; Chang-Ki Kang
Journal:  Healthcare (Basel)       Date:  2021-05-29

Review 10.  Keeping the Breath in Mind: Respiration, Neural Oscillations, and the Free Energy Principle.

Authors:  Asena Boyadzhieva; Ezgi Kayhan
Journal:  Front Neurosci       Date:  2021-06-29       Impact factor: 4.677

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