Convergent neural substrates of inattention in bipolar disorder patients and dopamine transporter‐deficient mice using the 5‐choice CPT

Bipolar disorder (BD) is a debilitating psychiatric illness affecting 2%‐5% of the population. Although mania is the cardinal feature of BD, inattention and related cognitive dysfunction are observed across all stages. Since cognitive dysfunction confers poor functional outcome in patients, understanding the relevant neural mechanisms remains key to developing novel‐targeted therapeutics.

[1]  S. Eickhoff,et al.  Dysfunction and Dysconnection in Cortical–Striatal Networks during Sustained Attention: Genetic Risk for Schizophrenia or Bipolar Disorder and its Impact on Brain Network Function , 2014, Front. Psychiatry.

[2]  J. Kelly,et al.  Impaired attention is central to the cognitive deficits observed in alpha 7 deficient mice , 2007, European Neuropsychopharmacology.

[3]  M. G. Perrucci,et al.  Impaired sustained attention in euthymic bipolar disorder patients and non‐affected relatives: an fMRI study , 2012, Bipolar disorders.

[4]  J. Os,et al.  Meta-analyses of cognitive functioning in euthymic bipolar patients and their first-degree relatives , 2007, Psychological Medicine.

[5]  Jared W. Young,et al.  Reverse translated and gold standard continuous performance tests predict global cognitive performance in schizophrenia , 2018, Translational Psychiatry.

[6]  Michael F. Green,et al.  Cognitive impairment and functional outcome in schizophrenia and bipolar disorder. , 2006, The Journal of clinical psychiatry.

[7]  W. Koek,et al.  The PARP inhibitor benzamide protects against kainate and NMDA but not AMPA lesioning of the mouse striatum in vivo , 2004, Brain Research.

[8]  Jared W. Young,et al.  The 5-Choice Continuous Performance Test: Evidence for a Translational Test of Vigilance for Mice , 2009, PloS one.

[9]  Sandra K Loo,et al.  Functional effects of the DAT1 polymorphism on EEG measures in ADHD. , 2003, Journal of the American Academy of Child and Adolescent Psychiatry.

[10]  A. Malhotra,et al.  Placebo-controlled adjunctive trial of pramipexole in patients with bipolar disorder: targeting cognitive dysfunction. , 2012, The Journal of clinical psychiatry.

[11]  Thomas S. Redick,et al.  CNTRICS final task selection: working memory. , 2009, Schizophrenia bulletin.

[12]  A. Minassian,et al.  The mania-like exploratory profile in genetic dopamine transporter mouse models is diminished in a familiar environment and reinstated by subthreshold psychostimulant administration , 2010, Pharmacology Biochemistry and Behavior.

[13]  M. Geyer,et al.  Reverse translation of the rodent 5C-CPT reveals that the impaired attention of people with schizophrenia is similar to scopolamine-induced deficits in mice , 2013, Translational Psychiatry.

[14]  É. Mezey,et al.  Dopaminergic characteristics of isolated parietal cells from rats , 1997, Journal of Physiology-Paris.

[15]  Mary L. Phillips,et al.  An fMRI study of attentional control in the context of emotional distracters in euthymic adults with bipolar disorder , 2012, Psychiatry Research: Neuroimaging.

[16]  G. Light,et al.  Neurophysiological Characterization of Attentional Performance Dysfunction in Schizophrenia Patients in a Reverse-Translated Task , 2017, Neuropsychopharmacology.

[17]  Cameron S. Carter,et al.  The neural circuitry supporting goal maintenance during cognitive control: a comparison of expectancy AX-CPT and dot probe expectancy paradigms , 2015, Cognitive, Affective, & Behavioral Neuroscience.

[18]  T. Bussey,et al.  Dissociable effects of AMPA-induced lesions of the vertical limb diagonal band of Broca on performance of the 5-choice serial reaction time task and on acquisition of a conditional visual discrimination , 1996, Behavioural Brain Research.

[19]  M. Geyer,et al.  Predictive animal models of mania: hits, misses and future directions , 2011, British journal of pharmacology.

[20]  V. Starcevic,et al.  Reliability of the Hamilton Rating Scale for Depression: A meta-analysis over a period of 49years , 2011, Psychiatry Research.

[21]  Jared W. Young,et al.  Bridging the bench to bedside gap: validation of a reverse-translated rodent continuous performance test using functional magnetic resonance imaging , 2013, Psychiatry Research: Neuroimaging.

[22]  J. Enkhuizen,et al.  Differential effects of dopamine transporter inhibitors in the rodent Iowa gambling task , 2012, Psychopharmacology.

[23]  Chandan J. Vaidya,et al.  Neural response to working memory load varies by dopamine transporter genotype in children , 2010, NeuroImage.

[24]  P. Najt,et al.  Right fronto-parietal dysfunction underlying spatial attention in bipolar disorder , 2013, Psychiatry Research.

[25]  A. Markou,et al.  Translational Rodent Paradigms to Investigate Neuromechanisms Underlying Behaviors Relevant to Amotivation and Altered Reward Processing in Schizophrenia. , 2015, Schizophrenia bulletin.

[26]  T. Robbins,et al.  CNTRICS final animal model task selection: Control of attention , 2013, Neuroscience & Biobehavioral Reviews.

[27]  J. Enkhuizen,et al.  Premature responses in the five-choice serial reaction time task reflect rodents’ temporal strategies: evidence from no-light and pharmacological challenges , 2016, Psychopharmacology.

[28]  Martin P Paulus,et al.  A reverse-translational study of dysfunctional exploration in psychiatric disorders: from mice to men. , 2009, Archives of general psychiatry.

[29]  F. Papaleo,et al.  Attentional Control in Adolescent Mice Assessed with a Modified Five Choice Serial Reaction Time Task , 2017, Scientific Reports.

[30]  Thomas E. Nichols,et al.  Can parametric statistical methods be trusted for fMRI based group studies? , 2015, 1511.01863.

[31]  F. Managò,et al.  Dopamine transporter (DAT) genetic hypofunction in mice produces alterations consistent with ADHD but not schizophrenia or bipolar disorder , 2017, Neuropharmacology.

[32]  M. Portella,et al.  Persistence of cognitive impairment and its negative impact on psychosocial functioning in lithium-treated, euthymic bipolar patients: a 6-year follow-up study , 2012, Psychological Medicine.

[33]  A. R. Little,et al.  Selective changes in gene expression in cortical regions sensitive to amphetamine during the neurodegenerative process. , 2004, Neurotoxicology.

[34]  D. Dougherty,et al.  Impulsivity and phase of illness in bipolar disorder. , 2003, Journal of affective disorders.

[35]  D1 receptor activation improves vigilance in rats as measured by the 5-choice continuous performance test , 2012, Psychopharmacology.

[36]  S. Frangou,et al.  Structural brain correlates of response inhibition in Bipolar Disorder I , 2008, Journal of psychopharmacology.

[37]  Melissa A. Cyders,et al.  Integration of impulsivity and positive mood to predict risky behavior: development and validation of a measure of positive urgency. , 2007, Psychological assessment.

[38]  T. Robbins,et al.  Impulsivity, Compulsivity, and Top-Down Cognitive Control , 2011, Neuron.

[39]  A. Sampson,et al.  Dopamine transporter immunoreactivity in monkey cerebral cortex: Regional, laminar, and ultrastructural localization , 2001, The Journal of comparative neurology.

[40]  S. Strakowski,et al.  Bipolar I disorder and major depressive disorder show similar brain activation during depression , 2014, Bipolar disorders.

[41]  M. Geyer,et al.  GlyT-1 Inhibition Attenuates Attentional But Not Learning or Motivational Deficits of the Sp4 Hypomorphic Mouse Model Relevant to Psychiatric Disorders , 2015, Neuropsychopharmacology.

[42]  A. Minassian,et al.  GBR 12909 administration as a mouse model of bipolar disorder mania: mimicking quantitative assessment of manic behavior , 2009, Psychopharmacology.

[43]  Ian H. Robertson,et al.  fMRI activation during response inhibition and error processing: The role of the DAT1 gene in typically developing adolescents and those diagnosed with ADHD , 2011, Neuropsychologia.

[44]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[45]  A. Minassian,et al.  Amphetamine improves mouse and human attention in the 5-choice continuous performance test , 2018, Neuropharmacology.

[46]  R. C. Young,et al.  A Rating Scale for Mania: Reliability, Validity and Sensitivity , 1978, British Journal of Psychiatry.

[47]  P. Balsam,et al.  Mice with Chronically Elevated Dopamine Exhibit Enhanced Motivation, but not Learning, for a Food Reward , 2006, Neuropsychopharmacology.

[48]  C. Depp,et al.  Longitudinal Study of Sustained Attention in Outpatients with Bipolar Disorder , 2014, Journal of the International Neuropsychological Society.

[49]  John Sharkey,et al.  Nicotine Improves Sustained Attention in Mice: Evidence for Involvement of the α7 Nicotinic Acetylcholine Receptor , 2004, Neuropsychopharmacology.

[50]  S. Silverstein,et al.  The Sustained Attention Test: A Measure of Attentional Disturbance , 1998 .

[51]  J. Neill,et al.  Rats tested after a washout period from sub-chronic PCP administration exhibited impaired performance in the 5-Choice Continuous Performance Test (5C-CPT) when the attentional load was increased , 2012, Neuropharmacology.

[52]  Youming Li,et al.  Traumatic brain injury reduces dopamine transporter protein expression in the rat frontal cortex , 2002, Neuroreport.

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

[54]  B R Rosen,et al.  Detection of dopaminergic neurotransmitter activity using pharmacologic MRI: Correlation with PET, microdialysis, and behavioral data , 1997, Magnetic resonance in medicine.

[55]  A. Sahgal Some limitations of indices derived from signal detection theory: evaluation of an alternative index for measuring bias in memory tasks , 2004, Psychopharmacology.

[56]  Jared W. Young,et al.  Nicotinic agonist-induced improvement of vigilance in mice in the 5-choice continuous performance test , 2013, Behavioural Brain Research.

[57]  P. DeRosse,et al.  The MATRICS Consensus Cognitive Battery in Patients with Bipolar I Disorder , 2011, Neuropsychopharmacology.

[58]  H. Happe,et al.  Postnatal development of the dopamine transporter: a quantitative autoradiographic study. , 1996, Brain research. Developmental brain research.

[59]  M. Geyer,et al.  Developing treatments for cognitive deficits in schizophrenia: The challenge of translation , 2015, Journal of psychopharmacology.

[60]  J. Enkhuizen,et al.  Reduced Dopamine Transporter Functioning Induces High-Reward Risk-Preference Consistent with Bipolar Disorder , 2014, Neuropsychopharmacology.

[61]  T. Suppes,et al.  Three times more days depressed than manic or hypomanic in both bipolar I and bipolar II disorder. , 2007, Bipolar disorders.

[62]  K. Nuechterlein Signal detection in vigilance tasks and behavioral attributes among offspring of schizophrenic mothers and among hyperactive children. , 1983, Journal of abnormal psychology.

[63]  Peter W. Frey,et al.  Sensitivity and responsivity measures for discrimination learning , 1973 .

[64]  E. Leibenluft,et al.  Neural correlates of cognitive flexibility in children at risk for bipolar disorder. , 2012, Journal of psychiatric research.

[65]  A. Young,et al.  Performance monitoring and executive control of attention in euthymic bipolar disorder: Employing the CPT-AX paradigm , 2013, Psychiatry Research.

[66]  M. Geyer,et al.  Evaluating the role of the alpha-7 nicotinic acetylcholine receptor in the pathophysiology and treatment of schizophrenia. , 2013, Biochemical pharmacology.

[67]  J. Overall The Brief Psychiatric Rating Scale in psychopharmacology research. , 1974 .

[68]  Ross D. Zafonte,et al.  Gender and environmental enrichment impact dopamine transporter expression after experimental traumatic brain injury , 2005, Experimental Neurology.

[69]  R. Hen,et al.  Hyperactivity and impaired response habituation in hyperdopaminergic mice. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[70]  T. Robbins,et al.  Assessing cognitive function in clinical trials of schizophrenia , 2010, Neuroscience & Biobehavioral Reviews.

[71]  Karly M. Turner,et al.  Attentional Processing in C57BL/6J Mice Exposed to Developmental Vitamin D Deficiency , 2012, PloS one.

[72]  M. Geyer,et al.  Brexpiprazole reduces hyperactivity, impulsivity, and risk-preference behavior in mice with dopamine transporter knockdown—a model of mania , 2017, Psychopharmacology.

[73]  J. Enkhuizen,et al.  Sleep deprivation impairs performance in the 5-choice continuous performance test: Similarities between humans and mice , 2014, Behavioural Brain Research.

[74]  Kevin S. Brown,et al.  Cooperation between the default mode network and the frontal–parietal network in the production of an internal train of thought , 2012, Brain Research.

[75]  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.

[76]  R. Kessler,et al.  Prevalence and correlates of bipolar spectrum disorder in the world mental health survey initiative. , 2011, Archives of general psychiatry.

[77]  Peter Gallagher,et al.  A meta-analysis of cognitive deficits in euthymic patients with bipolar disorder. , 2006, Journal of affective disorders.

[78]  M. Geyer,et al.  Chronic valproate attenuates some, but not all, facets of mania-like behaviour in mice. , 2013, The international journal of neuropsychopharmacology.

[79]  G. Muscettola,et al.  Differential expression of Homer 1 gene by acute and chronic administration of antipsychotics and dopamine transporter inhibitors in the rat forebrain , 2007, Synapse.

[80]  E. Leibenluft,et al.  A developmental study on the neural circuitry mediating response flexibility in bipolar disorder , 2013, Psychiatry Research: Neuroimaging.

[81]  Yanlin Wang,et al.  Restoration of cocaine stimulation and reward by reintroducing wild type dopamine transporter in adult knock-in mice with a cocaine-insensitive dopamine transporter , 2014, Neuropharmacology.

[82]  Catherine A. Sugar,et al.  Dopamine transporter knockdown mice in the behavioral pattern monitor: A robust, reproducible model for mania-relevant behaviors , 2017, Pharmacology Biochemistry and Behavior.