Association between rostral prefrontal cortical activity and functional outcome in first-episode psychosis: a longitudinal functional near-infrared spectroscopy study

BACKGROUND Few biomarkers can be used easily and noninvasively to measure clinical condition and future outcome in patients with first-episode psychosis (FEP). To develop such biomarker using multichannel functional near-infrared spectroscopy (fNIRS), cortical function in the prefrontal cortex was longitudinally measured during a verbal fluency task. METHODS Sixty-nine fNIRS measurements and 77 clinical assessments were obtained from 31 patients with FEP at baseline, 6-month, and 12-month follow-ups. Sixty measurements were obtained from 30 healthy controls matched for age, sex, and premorbid IQ. We initially tested signal changes for 12 months, and then investigated the relationship between fNIRS signals and clinical assessments. RESULTS Signal changes from baseline to 12-month follow-up were not evident in any group. Patients with FEP had significant positive correlation coefficients between 6-month fNIRS signals and the 12-month Global Assessment of Functioning (GAF) score in the left middle frontal gyrus (FDR-corrected p=.0016-.0052, r=.65-.59). fNIRS signals at the 12-month follow-up were associated with 12-month GAF score in the bilateral superior and middle frontal gyri (FDR-corrected p=.00085-.018, r=.72-.55), and with the difference between baseline and 12-month GAF scores in the right superior frontal gyrus (FDR-corrected p=.000067-.00012, r=.80-.78). These associations were significant even after controlling for demographic variables. No association between baseline fNIRS signals and later GAF scores was found. DISCUSSION fNIRS measurement can potentially be used as a biomarker to aid sequential assessment of neuro-clinical conditions through the early stage of psychosis.

[1]  Jim van Os,et al.  The environment and schizophrenia , 2010, Nature.

[2]  J. Lieberman,et al.  Antipsychotic drug effects on brain morphology in first-episode psychosis. , 2005, Archives of general psychiatry.

[3]  Nancy C. Andreasen,et al.  Progressive Brain Change in Schizophrenia: A Prospective Longitudinal Study of First-Episode Schizophrenia , 2011, Biological Psychiatry.

[4]  Archana K. Singh,et al.  Exploring the false discovery rate in multichannel NIRS , 2006, NeuroImage.

[5]  Janet B W Williams.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[6]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[7]  Kiyoto Kasai,et al.  Near-Infrared Spectroscopy in Schizophrenia: A Possible Biomarker for Predicting Clinical Outcome and Treatment Response , 2013, Front. Psychiatry.

[8]  Motohiro Okada,et al.  Intrasubject reproducibility of prefrontal cortex activities during a verbal fluency task over two repeated sessions using multi‐channel near‐infrared spectroscopy , 2009, Psychiatry and clinical neurosciences.

[9]  C. Pantelis,et al.  Prediction of functional outcome 18 months after a first psychotic episode: a proton magnetic resonance spectroscopy study. , 2006, Archives of general psychiatry.

[10]  J. Lieberman,et al.  Relationship between duration of untreated psychosis and outcome in first-episode schizophrenia: a critical review and meta-analysis. , 2005, The American journal of psychiatry.

[11]  Kiyoto Kasai,et al.  Prefrontal cortex activity during response inhibition associated with excitement symptoms in schizophrenia , 2011, Brain Research.

[12]  A. Mechelli,et al.  Functional integration between the posterior hippocampus and prefrontal cortex is impaired in both first episode schizophrenia and the at risk mental state. , 2009, Brain : a journal of neurology.

[13]  S. B. Hutton,et al.  Naturalistic follow-up of co-morbid substance use in schizophrenia: the West London first-episode study , 2007, Psychological Medicine.

[14]  I. Melle,et al.  Depressive symptoms in first episode psychosis: a one-year follow-up study , 2013, BMC Psychiatry.

[15]  Effects of sedative antidepressants on prefrontal cortex activity during verbal fluency task in healthy subjects: a near-infrared spectroscopy study , 2013, Psychopharmacology.

[16]  K. Kasai,et al.  Reduced but broader prefrontal activity in patients with schizophrenia during n-back working memory tasks: a multi-channel near-infrared spectroscopy study. , 2013, Journal of psychiatric research.

[17]  Aysenil Belger,et al.  Imaging frontostriatal function in ultra-high-risk, early, and chronic schizophrenia during executive processing. , 2005, Archives of general psychiatry.

[18]  Makoto Ito,et al.  Multichannel near-infrared spectroscopy in depression and schizophrenia: cognitive brain activation study , 2004, Biological Psychiatry.

[19]  Kiyoto Kasai,et al.  Distinct effects of duration of untreated psychosis on brain cortical activities in different treatment phases of schizophrenia: A multi-channel near-infrared spectroscopy study , 2014, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[20]  I. Hickie,et al.  Clinical Staging of Psychiatric Disorders: A Heuristic Framework for Choosing Earlier, Safer and more Effective Interventions , 2006, The Australian and New Zealand journal of psychiatry.

[21]  H. Fukuyama,et al.  Age-related cortical thinning in schizophrenia , 2011, Schizophrenia Research.

[22]  Kiyoto Kasai,et al.  Multiple-time replicability of near-infrared spectroscopy recording during prefrontal activation task in healthy men , 2007, Neuroscience Research.

[23]  U. Habel,et al.  The interaction of working memory and emotion in persons clinically at risk for psychosis: An fMRI pilot study , 2010, Schizophrenia Research.

[24]  Peter B. Jones,et al.  Association between duration of untreated psychosis and outcome in cohorts of first-episode patients: a systematic review. , 2005, Archives of general psychiatry.

[25]  M. Keshavan,et al.  Neuroprotective effects of cognitive enhancement therapy against gray matter loss in early schizophrenia: results from a 2-year randomized controlled trial. , 2010, Archives of general psychiatry.

[26]  I. Melle,et al.  Long-term follow-up of the TIPS early detection in psychosis study: effects on 10-year outcome. , 2012, The American journal of psychiatry.

[27]  J. Addington,et al.  The course of cognitive functioning in first episode psychosis: Changes over time and impact on outcome , 2005, Schizophrenia Research.

[28]  A. Malla,et al.  Symptoms, cognition, treatment adherence and functional outcome in first-episode psychosis , 2002, Psychological Medicine.

[29]  M. D’Esposito,et al.  Is the rostro-caudal axis of the frontal lobe hierarchical? , 2009, Nature Reviews Neuroscience.

[30]  Kiyoto Kasai,et al.  Association between severe dorsolateral prefrontal dysfunction during random number generation and earlier onset in schizophrenia , 2011, Clinical Neurophysiology.

[31]  Masato Fukuda,et al.  Reduced frontopolar activation during verbal fluency task in schizophrenia: A multi-channel near-infrared spectroscopy study , 2008, Schizophrenia Research.

[32]  Ann-Christine Ehlis,et al.  Functional near-infrared spectroscopy: A long-term reliable tool for measuring brain activity during verbal fluency , 2008, NeuroImage.

[33]  Dan J Stein,et al.  Toward a Global View of Alcohol, Tobacco, Cannabis, and Cocaine Use: Findings from the WHO World Mental Health Surveys , 2008, PLoS medicine.

[34]  A. Mackinnon,et al.  Depressive symptoms in first episode schizophrenia spectrum disorder , 2012, Schizophrenia Research.

[35]  A. Yung,et al.  Prediction of a single psychotic episode: A 7.5-year, prospective study in first-episode psychosis , 2011, Schizophrenia Research.

[36]  H. Yamasue,et al.  A multimodal approach to investigate biomarkers for psychosis in a clinical setting: The integrative neuroimaging studies in schizophrenia targeting for early intervention and prevention (IN-STEP) project , 2013, Schizophrenia Research.

[37]  A. Egerton,et al.  Transition to psychosis associated with prefrontal and subcortical dysfunction in ultra high-risk individuals. , 2012, Schizophrenia bulletin.

[38]  Philip K. McGuire,et al.  Neural correlates of executive function and working memory in the ‘at-risk mental state’ , 2007, British Journal of Psychiatry.

[39]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[40]  Masako Okamoto,et al.  Virtual spatial registration of stand-alone fNIRS data to MNI space , 2007, NeuroImage.

[41]  W. Fleischhacker,et al.  Symptomatic remission and neurocognitive functioning in patients with schizophrenia , 2011, Psychological Medicine.

[42]  Tyrone D. Cannon,et al.  Prediction of psychosis in youth at high clinical risk: a multisite longitudinal study in North America. , 2008, Archives of general psychiatry.

[43]  J. O. Johannessen,et al.  Neurocognitive development in first episode psychosis 5years follow-up: Associations between illness severity and cognitive course , 2013, Schizophrenia Research.

[44]  Andrew Simmons,et al.  Cortical folding defects as markers of poor treatment response in first-episode psychosis. , 2013, JAMA psychiatry.

[45]  Masato Fukuda,et al.  Different hemodynamic response patterns in the prefrontal cortical sub-regions according to the clinical stages of psychosis , 2011, Schizophrenia Research.

[46]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.