Brain regions associated with olfactory dysfunction in first episode psychosis patients

Abstract Objectives Olfactory dysfunction is reproducibly reported in psychotic disorders, particularly in association with negative symptoms. The superior frontal gyrus (SFG) has been frequently studied in patients with psychotic disorders, in particular with their associations with negative symptoms. The relationship between olfactory functions and brain structure has been studied in healthy controls (HCs). Nevertheless, the studies with patients with psychotic disorders are limited. Here we report the olfactory-brain relationship in a first episode psychosis (FEP) cohort through both hypothesis-driven (centred on the SFG) and data-driven approaches. Methods Using data from 88 HCs and 76 FEP patients, we evaluated the correlation between olfactory functions and structural/resting-state functional magnetic resonance imaging (MRI) data. Results We found a significant correlation between the left SFG volume and odour discrimination in FEP patients, but not in HCs. We also observed a significant correlation between rs-fMRI connectivity involving the left SFG and odour discrimination in FEP patients, but not in HCs. The data-driven approach didn’t observe any significant correlations, possibly due to insufficient statistical power. Conclusion The left SFG may be a promising brain region in the context of olfactory dysfunction and negative symptoms in FEP.

[1]  M. Miller,et al.  A comparative neuroimaging perspective of olfaction and higher-order olfactory processing: on health and disease. , 2021, Seminars in cell & developmental biology.

[2]  J. Hua,et al.  Volumetric alteration of olfactory bulb and immune-related molecular changes in olfactory epithelium in first episode psychosis patients , 2021, Schizophrenia Research.

[3]  Paul J. Harrison,et al.  6-month neurological and psychiatric outcomes in 236 379 survivors of COVID-19: a retrospective cohort study using electronic health records , 2021, The Lancet Psychiatry.

[4]  Johnny T. C. Hsu,et al.  Multimodal MRI assessment for first episode psychosis: A major change in the thalamus and an efficient stratification of a subgroup , 2020, Human brain mapping.

[5]  Henry M. Quillian,et al.  Association of Missense Mutation in FOLH1 With Decreased NAAG Levels and Impaired Working Memory Circuitry and Cognition. , 2020, The American journal of psychiatry.

[6]  C. Conrad,et al.  Olfactory transmucosal SARS-CoV-2 invasion as a port of central nervous system entry in individuals with COVID-19 , 2020, Nature Neuroscience.

[7]  Paul J. Harrison,et al.  Bidirectional associations between COVID-19 and psychiatric disorder: retrospective cohort studies of 62 354 COVID-19 cases in the USA , 2020, The Lancet Psychiatry.

[8]  S. Farhadian,et al.  Neuropathogenesis and Neurologic Manifestations of the Coronaviruses in the Age of Coronavirus Disease 2019: A Review. , 2020, JAMA neurology.

[9]  A. Roy,et al.  Functional connectivity of the anterior insula associated with intolerance of uncertainty in youth , 2020, Cognitive, Affective, & Behavioral Neuroscience.

[10]  R. Chan,et al.  Impaired olfactory identification and hedonic judgment in schizophrenia patients with prominent negative symptoms , 2019, Cognitive neuropsychiatry.

[11]  Feng Liu,et al.  Brain structural abnormalities as potential markers for detecting individuals with ultra-high risk for psychosis: A systematic review and meta-analysis , 2019, Schizophrenia Research.

[12]  Johnny T. C. Hsu,et al.  Relationship between neuropsychological behavior and brain white matter in first-episode psychosis , 2019, Schizophrenia Research.

[13]  M. Achterberg,et al.  Genetic and environmental influences on MRI scan quantity and quality , 2019, Developmental Cognitive Neuroscience.

[14]  Jennifer M. Coughlin,et al.  Assessing Brain Metabolism With 7-T Proton Magnetic Resonance Spectroscopy in Patients With First-Episode Psychosis , 2019, JAMA psychiatry.

[15]  M. Kotlicka‐Antczak,et al.  Odor perception and hedonics in chronic schizophrenia and in first episode psychosis , 2019, Neuropsychiatric disease and treatment.

[16]  A. Sawa,et al.  Contributions of Olfactory and Neuropsychological Assessment to the Diagnosis of First-Episode Schizophrenia , 2019, Neuropsychology.

[17]  Adrian Preda,et al.  Cortical Brain Abnormalities in 4474 Individuals With Schizophrenia and 5098 Control Subjects via the Enhancing Neuro Imaging Genetics Through Meta Analysis (ENIGMA) Consortium , 2018, Biological Psychiatry.

[18]  Junmei Hu,et al.  Olfactory impairment in first-episode schizophrenia: a case-control study, and sex dimorphism in the relationship between olfactory impairment and psychotic symptoms , 2018, BMC Psychiatry.

[19]  J. Mullol,et al.  Olfactory Dysfunction in Neurodegenerative Diseases , 2018, Current Allergy and Asthma Reports.

[20]  J. Rushworth,et al.  Olfactory Dysfunction as a Global Biomarker for Sniffing out Alzheimer’s Disease: A Meta-Analysis , 2018, Biosensors.

[21]  A. Sawa,et al.  Olfactory Functioning in First-Episode Psychosis , 2018, Schizophrenia bulletin.

[22]  R. Pessoa,et al.  Olfactory dysfunction in Alzheimer’s disease Systematic review and meta-analysis , 2018, Dementia & neuropsychologia.

[23]  T. Ikuta,et al.  Disrupted Olfactory Integration in Schizophrenia: Functional Connectivity Study , 2017, The international journal of neuropsychopharmacology.

[24]  C. Li,et al.  Altered Functional Connectivity of the Basal Nucleus of Meynert in Mild Cognitive Impairment: A Resting-State fMRI Study , 2017, Alzheimer's & Dementia.

[25]  Jennifer M. Coughlin,et al.  Decoupling of Brain Temperature and Glutamate in Recent Onset of Schizophrenia: A 7T Proton Magnetic Resonance Spectroscopy Study. , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[26]  D. Strzelecki,et al.  Olfactory identification in patients with schizophrenia – the influence of β-endorphin and calcitonin gene-related peptide concentrations , 2017, European Psychiatry.

[27]  M. Karbownik,et al.  Deficits in the identification of pleasant odors predict the transition of an at-risk mental state to psychosis , 2017, Schizophrenia Research.

[28]  Dan Wu,et al.  MRICloud: Delivering High-Throughput MRI Neuroinformatics as Cloud-Based Software as a Service , 2016, Computing in Science & Engineering.

[29]  Emmanuelle Courtiol,et al.  Neural Representation of Odor-Guided Behavior in the Rat Olfactory Thalamus , 2016, The Journal of Neuroscience.

[30]  Michael I. Miller,et al.  Resource atlases for multi-atlas brain segmentations with multiple ontology levels based on T1-weighted MRI , 2016, NeuroImage.

[31]  Karin E. Borgmann-Winter,et al.  Olfactory processing in schizophrenia, non-ill first-degree family members, and young people at-risk for psychosis , 2014, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[32]  P. Barta,et al.  Reduced anterior cingulate gray matter volume and thickness in subjects with deficit schizophrenia , 2013, Schizophrenia Research.

[33]  H. Bickeböller,et al.  Odor naming and interpretation performance in 881 schizophrenia subjects: association with clinical parameters , 2013, BMC Psychiatry.

[34]  Xiaoying Tang,et al.  Bayesian Parameter Estimation and Segmentation in the Multi-Atlas Random Orbit Model , 2013, PloS one.

[35]  Michael I. Miller,et al.  Atlas-based analysis of resting-state functional connectivity: Evaluation for reproducibility and multi-modal anatomy–function correlation studies , 2012, NeuroImage.

[36]  A. Cohen,et al.  Olfaction, “olfiction,” and the schizophrenia-spectrum: An updated meta-analysis on identification and acuity , 2012, Schizophrenia Research.

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

[38]  Sohee Park,et al.  Olfactory identification and preference in bipolar disorder and schizophrenia , 2011, European Archives of Psychiatry and Clinical Neuroscience.

[39]  W. Cook,et al.  Neuropsychological profiles in individuals at clinical high risk for psychosis: Relationship to psychosis and intelligence , 2010, Schizophrenia Research.

[40]  G. Pearlson,et al.  Gray-matter abnormalities in deficit schizophrenia , 2010, Schizophrenia Research.

[41]  Claire Martin,et al.  Directional coupling from the olfactory bulb to the hippocampus during a go/no-go odor discrimination task. , 2010, Journal of neurophysiology.

[42]  A. Sawa,et al.  Negative symptoms of schizophrenia correlate with impairment on the University of Pennsylvania Smell Identification Test , 2010, Neuroscience Research.

[43]  B. Turetsky,et al.  An odor-specific threshold deficit implicates abnormal intracellular cyclic AMP signaling in schizophrenia. , 2009, The American journal of psychiatry.

[44]  E. Barkai,et al.  Olfactory Learning-Induced Long-Lasting Enhancement of Descending and Ascending Synaptic Transmission to the Piriform Cortex , 2008, The Journal of Neuroscience.

[45]  B. Turetsky,et al.  Olfactory Functioning in Schizophrenia: Relationship to Clinical, Neuropsychological, and Volumetric MRI Measures , 2006, Journal of clinical and experimental neuropsychology.

[46]  R. Malach,et al.  When the Brain Loses Its Self: Prefrontal Inactivation during Sensorimotor Processing , 2006, Neuron.

[47]  P. Szeszko,et al.  Olfactory functions and volumetric measures of orbitofrontal and limbic regions in schizophrenia , 2005, Schizophrenia Research.

[48]  David R Roalf,et al.  Decrements in volume of anterior ventromedial temporal lobe and olfactory dysfunction in schizophrenia. , 2003, Archives of general psychiatry.

[49]  C. Pantelis,et al.  Impairment of olfactory identification ability in individuals at ultra-high risk for psychosis who later develop schizophrenia. , 2003, The American journal of psychiatry.

[50]  G. Schoenbaum,et al.  Neural Encoding in Ventral Striatum during Olfactory Discrimination Learning , 2003, Neuron.

[51]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.

[52]  Charles L. Wilson,et al.  Electric current stimulates laughter , 1998, Nature.

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

[54]  G Kobal,et al.  "Sniffin' sticks": screening of olfactory performance. , 1996, Rhinology.

[55]  L. Kopala,et al.  Olfactory deficits in schizophrenia are not a function of task complexity , 1995, Schizophrenia Research.

[56]  Karin E. Borgmann-Winter,et al.  Meta-analysis of olfactory function in schizophrenia, first-degree family members, and youths at-risk for psychosis. , 2014, Schizophrenia bulletin.

[57]  Charlton Cheung,et al.  Gray matter in first-episode schizophrenia before and after antipsychotic drug treatment. Anatomical likelihood estimation meta-analyses with sample size weighting. , 2011, Schizophrenia bulletin.

[58]  T. Goldberg,et al.  The frontal lobes and schizophrenia. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[59]  J. Gorman,et al.  Odor discrimination deficits in schizophrenia: association with eye movement dysfunction. , 1994, The Journal of neuropsychiatry and clinical neurosciences.