When to collect resting-state data: The influence of odor on post-task resting-state connectivity

ABSTRACT The human brain networks at rest represent spontaneous activity that is highly correlated between different brain regions. Previous studies have shown that these resting‐state networks are flexible and dynamic, and they can be affected by performance of different types of tasks. Moreover, it has been suggested that the re‐activation of a task‐related brain network during rest promotes learning and improves the expertise on that task. However, it is still unclear whether the presence of different sensory information in the on‐task state affects functional connectivity in subsequent resting‐state fMRI even though the perception of the sensory information did not induce significant behavioral effects. To clarify this issue, we compared pre‐ and post‐task resting‐state fMRI of two groups of participants performing the same task either with an odor context (ODOR group) or without an odor context (AIR group). Seed‐based functional connectivity analyses were performed with orbitofrontal cortex, piriform cortex and working‐memory core network as seeds. The results showed that an odor context presented during an encoding task induced significant changes in the functional connectivity only within the olfactory network of the post‐task resting‐state compared to the same post‐task situation without previous odor context. No significant difference in functional connectivity were found for the working‐memory core network. This evidence emphasizes how the sensory context, in which a task is performed, is relevant for understanding the observed changes of functional connectivity during rest.

[1]  H. Nusbaum,et al.  Task-dependent organization of brain regions active during rest , 2009, Proceedings of the National Academy of Sciences.

[2]  Jessica R. Chamberland,et al.  Odor Valence Linearly Modulates Attractiveness, but Not Age Assessment, of Invariant Facial Features in a Memory-Based Rating Task , 2014, PloS one.

[3]  M. Seghier The Angular Gyrus , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[4]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[5]  Paul Sajda,et al.  Brain dynamics of post‐task resting state are influenced by expertise: Insights from baseball players , 2016, Human brain mapping.

[6]  R. Zatorre,et al.  Structure and function of auditory cortex: music and speech , 2002, Trends in Cognitive Sciences.

[7]  P. Dalton Psychophysical and behavioral characteristics of olfactory adaptation. , 2000, Chemical senses.

[8]  G. Zucco,et al.  Unconscious odour conditioning 25 years later: Revisiting and extending ‘Kirk-Smith, Van Toller and Dodd’ , 2009 .

[9]  V. Schöpf,et al.  A systematic investigation of the invariance of resting-state network patterns: is resting-state fMRI ready for pre-surgical planning? , 2013, Front. Hum. Neurosci..

[10]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[11]  K. Onoda,et al.  Different pre‐scanning instructions induce distinct psychological and resting brain states during functional magnetic resonance imaging , 2018, The European journal of neuroscience.

[12]  R. A. de Wijk,et al.  Habituation and adaptation to odors in humans , 2017, Physiology & Behavior.

[13]  Nicholas A. Ketz,et al.  Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences , 2010, Neuron.

[14]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[15]  J. Chébat,et al.  Impact of ambient odors on mall shoppers' emotions, cognition, and spending: A test of competitive causal theories , 2003 .

[16]  L. Yao,et al.  Motor Imagery Learning Modulates Functional Connectivity of Multiple Brain Systems in Resting State , 2014, PloS one.

[17]  P. Zhu,et al.  Exocytosis from large dense cored vesicles outside the active synaptic zones of terminals within the trigeminal subnucleus caudalis: A possible mechanism for neuropeptide release , 1986, Neuroscience.

[18]  Indistinguishable odour enantiomers: Differences between peripheral and central-nervous electrophysiological responses , 2017, Scientific Reports.

[19]  A. Mackay-Sim,et al.  Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects , 2007, European Archives of Oto-Rhino-Laryngology.

[20]  Ning Zhong,et al.  Changes in the brain intrinsic organization in both on-task state and post-task resting state , 2012, NeuroImage.

[21]  Graeme D. Jackson,et al.  Resting state functional connectivity changes induced by prior brain state are not network specific , 2015, NeuroImage.

[22]  Angela R. Laird,et al.  Modelling neural correlates of working memory: A coordinate-based meta-analysis , 2012, NeuroImage.

[23]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[24]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[25]  Johan N Lundström,et al.  Central Processing of the Chemical Senses: an Overview. , 2011, ACS chemical neuroscience.

[26]  C. Zelano,et al.  Characterizing functional pathways of the human olfactory system , 2019, eLife.

[27]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[28]  Fang Xie,et al.  Olfactory Mucosa: Composition, Enzymatic Localization, and Metabolism , 2015 .

[29]  F. Fischmeister,et al.  Olfactory training induces changes in regional functional connectivity in patients with long-term smell loss , 2015, NeuroImage: Clinical.

[30]  R. Rumiati,et al.  Relative Contribution of Odour Intensity and Valence to Moral Decisions , 2017, Perception.

[31]  V. Schöpf,et al.  Functional brain networks during picture encoding and recognition in different odor contexts , 2017, Behavioural Brain Research.

[32]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[33]  C. Grady,et al.  Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation , 2009, Neuropsychologia.

[34]  T. Hummel,et al.  Electro-olfactogram Responses Before and After Aversive Olfactory Conditioning in Humans , 2018, Neuroscience.

[35]  Janina Seubert,et al.  Orbitofrontal cortex and olfactory bulb volume predict distinct aspects of olfactory performance in healthy subjects. , 2013, Cerebral cortex.

[36]  A. Arshamian,et al.  Odor-Based Context Dependent Memory , 2017 .

[37]  Todd B. Parrish,et al.  Impact of signal‐to‐noise on functional MRI , 2000 .

[38]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[39]  David J. Freedman,et al.  Task Dependence of Visual and Category Representations in Prefrontal and Inferior Temporal Cortices , 2014, The Journal of Neuroscience.

[40]  U. Castiello,et al.  Implicit olfactory processing attenuates motor disturbances in idiopathic Parkinson's disease , 2013, Cortex.

[41]  T. Hummel,et al.  'Sniffin' sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. , 1997, Chemical senses.

[42]  Cheryl L. Grady,et al.  Task-Related Effects on the Temporal and Spatial Dynamics of Resting-State Functional Connectivity in the Default Network , 2010, PloS one.

[43]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[44]  David H. Zald,et al.  On the scent of human olfactory orbitofrontal cortex: Meta-analysis and comparison to non-human primates , 2005, Brain Research Reviews.

[45]  S. Boesveldt,et al.  Methods for building an inexpensive computer-controlled olfactometer for temporally-precise experiments. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[46]  C. Philpott,et al.  Olfactory clearance: what time is needed in clinical practice? , 2007, The Journal of Laryngology & Otology.

[47]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[48]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.