Psychopharmacology

, Volume 234, Issue 13, pp 2047–2062 | Cite as

A schizophrenia relevant 5-Choice Serial Reaction Time Task for mice assessing broad monitoring, distractibility and impulsivity

  • Huiping Huang
  • Simone Guadagna
  • Maddalena Mereu
  • Mariasole Ciampoli
  • Giacomo Pruzzo
  • Theresa Ballard
  • Francesco Papaleo
Original Investigation

Abstract

The 5-Choice Serial Reaction Time Task (5-CSRTT) is an automated test for rodents allowing the assessment of multiple cognitive measures. Originally designed to assess cognitive deficits relevant to attention deficit hyperactivity disorder, it has been widely used in the investigation of neural systems of attention. In the current study, we have set up a modified version, which reduced the training phase to only 8–9 days with minimal food deprivation and without single-housing. Furthermore, based on evidence that patients with schizophrenia are more impaired in broad monitoring abilities than in sustained attention, we successfully developed a protocol replicating the Spatial Attentional Resource Allocation Task (SARAT), used in humans to assess broad monitoring. During this task, when the target appeared at a single pre-cued location, mice selectively responded faster. Instead, increasing the number of validly cued locations proportionately decreased accuracy. We then validated a protocol which is relevant for neuropsychiatric disorders in which additional irrelevant pre-cue lights selectively disrupted attention (distractibility). Finally, we improved previously used protocols changing inter-trial intervals from 5 to 7 s by randomly presenting this shift only in 20% of the trials. This resulted in a selective effect on premature responses (impulsivity), with important implications for schizophrenia as well as for other mental disorders. Therefore, this revised 5-CSRTT reduced training and stress on the animals while selectively measuring different cognitive functions with translational validity to schizophrenia and other psychiatric disorders.

Keywords

Attentional control Cognition Behaviour Operant task Schizophrenia 

Notes

Acknowledgements

We thank Dr. M. Morini, C. Chiabrera, A. Parodi, R. Navone and T. Luchetta for their excellent technical assistance.

Compliance with ethical standards

All procedures were approved by the Italian Ministry of Health (permit n. 230/2009-B) and strictly adhere to the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health.

Funding and disclosure

This research was supported by the Istituto Italiano di Tecnologia, the 2015 NARSAD Independent Investigator Grant and the RPF Roche program. The authors declare that they have no financial conflicts of interest and that they have nothing to disclose.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

213_2017_4611_MOESM1_ESM.pptx (82 kb)
ESM 1(PPTX 81 kb)

References

  1. Amitai N, Markou A (2009) Increased impulsivity and disrupted attention induced by repeated phencyclidine are not attenuated by chronic quetiapine treatment. Pharmacol Biochem Behav 93:248–257CrossRefPubMedGoogle Scholar
  2. Amitai N, Markou A (2011) Comparative effects of different test day challenges on performance in the 5-choice serial reaction time task. Behav Neurosci 125:764–774CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amitai N, Semenova S, Markou A (2007) Cognitive-disruptive effects of the psychotomimetic phencyclidine and attenuation by atypical antipsychotic medications in rats. Psychopharmacology 193:521–537CrossRefPubMedGoogle Scholar
  4. Amr M, Volpe FM (2013) Relationship between anhedonia and impulsivity in schizophrenia, major depression and schizoaffective disorder. Asian J Psychiatr 6:577–580CrossRefPubMedGoogle Scholar
  5. Balducci C, Nurra M, Pietropoli A, Samanin R, Carli M (2003) Reversal of visual attention dysfunction after AMPA lesions of the nucleus basalis magnocellularis (NBM) by the cholinesterase inhibitor donepezil and by a 5-HT1A receptor antagonist WAY 100635. Psychopharmacology 167:28–36CrossRefPubMedGoogle Scholar
  6. Barbelivien A, Ruotsalainen S, Sirvio J (2001) Metabolic alterations in the prefrontal and cingulate cortices are related to behavioral deficits in a rodent model of attention-deficit hyperactivity disorder. Cereb Cortex 11:1056–1063CrossRefPubMedGoogle Scholar
  7. Bari A, Dalley JW, Robbins TW (2008) The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat Protoc 3:759–767CrossRefPubMedGoogle Scholar
  8. Bayless DW, Darling JS, Stout WJ, Daniel JM (2012) Sex differences in attentional processes in adult rats as measured by performance on the 5-choice serial reaction time task. Behav Brain Res 235:48–54CrossRefPubMedGoogle Scholar
  9. Beck LH, Bransome ED Jr, Mirsky AF, Rosvold HE, Sarason I (1956) A continuous performance test of brain damage. J Consult Psychol 20:343–350CrossRefPubMedGoogle Scholar
  10. Bowen L, Wallace CJ, Glynn SM, Nuechterlein KH, Lutzker JR, Kuehnel TG (1994) Schizophrenic individuals’ cognitive functioning and performance in interpersonal interactions and skills training procedures. J Psychiatr Res 28:289–301CrossRefPubMedGoogle Scholar
  11. Burton CL, Fletcher PJ (2012) Age and sex differences in impulsive action in rats: the role of dopamine and glutamate. Behav Brain Res 230:21–33CrossRefPubMedGoogle Scholar
  12. Bushnell PJ (2001) Assessing attention in rats. In: Buccafusco JJ (ed) Methods of behavior analysis in neuroscience. CRC Press, Boca Raton, pp 111–122Google Scholar
  13. Carli M, Calcagno E, Mainini E, Arnt J, Invernizzi RW (2011a) Sertindole restores attentional performance and suppresses glutamate release induced by the NMDA receptor antagonist CPP. Psychopharmacology 214:625–637CrossRefPubMedGoogle Scholar
  14. Carli M, Calcagno E, Mainolfi P, Mainini E, Invernizzi RW (2011b) Effects of aripiprazole, olanzapine, and haloperidol in a model of cognitive deficit of schizophrenia in rats: relationship with glutamate release in the medial prefrontal cortex. Psychopharmacology 214:639–652CrossRefPubMedGoogle Scholar
  15. Carli M, Robbins TW, Evenden JL, Everitt BJ (1983) Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal. Behav Brain Res 9:361–380CrossRefPubMedGoogle Scholar
  16. Carter CS, Barch DM (2007) Cognitive neuroscience-based approaches to measuring and improving treatment effects on cognition in schizophrenia: the CNTRICS initiative. Schizophr Bull 33:1131–1137CrossRefPubMedPubMedCentralGoogle Scholar
  17. Carter CS, Barch DM, Buchanan RW, Bullmore E, Krystal JH, Cohen J, Geyer M, Green M, Nuechterlein KH, Robbins T, Silverstein S, Smith EE, Strauss M, Wykes T, Heinssen R (2008) Identifying cognitive mechanisms targeted for treatment development in schizophrenia: an overview of the first meeting of the Cognitive Neuroscience Treatment Research to Improve Cognition in Schizophrenia Initiative. Biol Psychiatry 64:4–10CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chamberlain SR, Muller U, Robbins TW, Sahakian BJ (2006) Neuropharmacological modulation of cognition. Curr Opin Neurol 19:607–612CrossRefPubMedGoogle Scholar
  19. Chudasama Y, Passetti F, Rhodes SE, Lopian D, Desai A, Robbins TW (2003) Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav Brain Res 146:105–119CrossRefPubMedGoogle Scholar
  20. Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28:771–784CrossRefPubMedGoogle Scholar
  21. Dalley JW, Everitt Barry J, Robbins Trevor W (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69:680–694CrossRefPubMedGoogle Scholar
  22. Dalley JW, Fryer TD, Brichard L, Robinson ES, Theobald DE, Laane K, Pena Y, Murphy ER, Shah Y, Probst K, Abakumova I, Aigbirhio FI, Richards HK, Hong Y, Baron JC, Everitt BJ, Robbins TW (2007) Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315:1267–1270CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dalley JW, Theobald DE, Pereira EA, Li PM, Robbins TW (2002) Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity. Psychopharmacology 164:329–340CrossRefPubMedGoogle Scholar
  24. Davies W (2014) Sex differences in attention deficit hyperactivity disorder: candidate genetic and endocrine mechanisms. Front Neuroendocrinol 35:331–346CrossRefPubMedGoogle Scholar
  25. Davies W, Humby T, Kong W, Otter T, Burgoyne PS, Wilkinson LS (2009) Converging pharmacological and genetic evidence indicates a role for steroid sulfatase in attention. Biol Psychiatry 66:360–367CrossRefPubMedPubMedCentralGoogle Scholar
  26. Davies W, Humby T, Trent S, Eddy JB, Ojarikre OA, Wilkinson LS (2014) Genetic and pharmacological modulation of the steroid sulfatase axis improves response control; comparison with drugs used in ADHD. Neuropsychopharmacology 39:2622–2632CrossRefPubMedPubMedCentralGoogle Scholar
  27. de Bruin NM, Fransen F, Duytschaever H, Grantham C, Megens AA (2006) Attentional performance of (C57BL/6Jx129Sv)F2 mice in the five-choice serial reaction time task. Physiol Behav 89:692–703CrossRefPubMedGoogle Scholar
  28. Demeter E, Sarter M, Lustig C (2008) Rats and humans paying attention: cross-species task development for translational research. Neuropsychology 22:787–799CrossRefPubMedPubMedCentralGoogle Scholar
  29. Eagle DM, Baunez C (2010) Is there an inhibitory-response-control system in the rat? Evidence from anatomical and pharmacological studies of behavioral inhibition. Neurosci Biobehav Rev 34:50–72CrossRefPubMedPubMedCentralGoogle Scholar
  30. Escera C, Alho K, Schroger E, Winkler I (2000) Involuntary attention and distractibility as evaluated with event-related brain potentials. Audiol Neurootol 5:151–166CrossRefPubMedGoogle Scholar
  31. Fassbender C, Zhang H, Buzy WM, Cortes CR, Mizuiri D, Beckett L, Schweitzer JB (2009) A lack of default network suppression is linked to increased distractibility in ADHD. Brain Res 1273:114–128CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ford JM, Pfefferbaum A, Roth W (1992) P3 and Schizophreniaa. Ann N Y Acad Sci 658:146–162CrossRefPubMedGoogle Scholar
  33. Gendle MH, White TL, Strawderman M, Mactutus CF, Booze RM, Levitsky DA, Strupp BJ (2004) Enduring effects of prenatal cocaine exposure on selective attention and reactivity to errors: evidence from an animal model. Behav Neurosci 118:290–297CrossRefPubMedGoogle Scholar
  34. Gmehlin D, Fuermaier AB, Walther S, Tucha L, Koerts J, Lange KW, Tucha O, Weisbrod M, Aschenbrenner S (2016) Attentional lapses of adults with attention deficit hyperactivity disorder in tasks of sustained attention. Arch Clin Neuropsychol 31:343–357CrossRefPubMedGoogle Scholar
  35. Gold JM, Thaker GK (2002) Current progress in schizophrenia research: cognitive phenotypes of schizophrenia: attention. J Nerv Ment Dis 190:638–639CrossRefPubMedGoogle Scholar
  36. Gray BE, Hahn B, Robinson B, Harvey A, Leonard CJ, Luck SJ, Gold JM (2014) Relationships between divided attention and working memory impairment in people with schizophrenia. Schizophr Bull 40:1462–1471CrossRefPubMedPubMedCentralGoogle Scholar
  37. Greco B, Carli M (2006) Reduced attention and increased impulsivity in mice lacking NPY Y2 receptors: relation to anxiolytic-like phenotype. Behav Brain Res 169:325–334CrossRefPubMedGoogle Scholar
  38. Green MF, Kern RS, Heaton RK (2004) Longitudinal studies of cognition and functional outcome in schizophrenia: implications for MATRICS. Schizophr Res 72:41–51CrossRefPubMedGoogle Scholar
  39. Grillon C, Courchesne E, Ameli R, Geyer MA, Braff DL (1990) Increased distractibility in schizophrenic patients. Electrophysiologic and behavioral evidence. Arch Gen Psychiatry 47:171–179CrossRefPubMedGoogle Scholar
  40. Gut-Fayand A, Dervaux A, Olie JP, Loo H, Poirier MF, Krebs MO (2001) Substance abuse and suicidality in schizophrenia: a common risk factor linked to impulsivity. Psychiatry Res 102:65–72CrossRefPubMedGoogle Scholar
  41. Hahn B, Harvey AN, Gold JM, Fischer BA, Keller WR, Ross TJ, Stein EA (2016) Hyperdeactivation of the default mode network in people with schizophrenia when focusing attention in space. Schizophr Bull 28Google Scholar
  42. Hahn B, Robinson BM, Harvey AN, Kaiser ST, Leonard CJ, Luck SJ, Gold JM (2012) Visuospatial attention in schizophrenia: deficits in broad monitoring. J Abnorm Psychol 121:119–128CrossRefPubMedGoogle Scholar
  43. Hahn B, Ross TJ, Stein EA (2006) Neuroanatomical dissociation between bottom-up and top-down processes of visuospatial selective attention. NeuroImage 32:842–853CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hahn B, Shoaib M, Stolerman IP (2002) Nicotine-induced enhancement of attention in the five-choice serial reaction time task: the influence of task demands. Psychopharmacology 162:129–137CrossRefPubMedGoogle Scholar
  45. Hahn B, Stolerman IP (2002) Nicotine-induced attentional enhancement in rats: effects of chronic exposure to nicotine. Neuropsychopharmacology 27:712–722CrossRefPubMedGoogle Scholar
  46. Harrison AA, Everitt BJ, Robbins TW (1997) Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: interactions with dopaminergic mechanisms. Psychopharmacology 133:329–342CrossRefPubMedGoogle Scholar
  47. Heaton RK, Gladsjo JA, Palmer BW, Kuck J, Marcotte TD, Jeste DV (2001) Stability and course of neuropsychological deficits in schizophrenia. Arch Gen Psychiatry 58:24–32CrossRefPubMedGoogle Scholar
  48. Holden C (2005) Sex and the suffering brain. Science 308:1574–1574CrossRefPubMedGoogle Scholar
  49. Hoptman MJ, Volavka J, Johnson G, Weiss E, Bilder RM, Lim KO (2002) Frontal white matter microstructure, aggression, and impulsivity in men with schizophrenia: a preliminary study. Biol Psychiatry 52:9–14CrossRefPubMedGoogle Scholar
  50. Humby T, Laird FM, Davies W, Wilkinson LS (1999) Visuospatial attentional functioning in mice: interactions between cholinergic manipulations and genotype. Eur J Neurosci 11:2813–2823CrossRefPubMedGoogle Scholar
  51. Ilott NE, Schneider T, Mill J, Schalkwyk L, Brolese G, Bizarro L, Stolerman IP, Dempster E, Asherson P (2014) Long-term effects of gestational nicotine exposure and food-restriction on gene expression in the striatum of adolescent rats. PLoS One 9(2):e88896. doi:10.1371/journal.pone.0088896
  52. Inglis WL, Olmstead MC, Robbins TW (2001) Selective deficits in attentional performance on the 5-choice serial reaction time task following pedunculopontine tegmental nucleus lesions. Behav Brain Res 123:117–131CrossRefPubMedGoogle Scholar
  53. Irimia C, Wiskerke J, Natividad LA, Polis IY, de Vries TJ, Pattij T, Parsons LH (2015) Increased impulsivity in rats as a result of repeated cycles of alcohol intoxication and abstinence. Addict Biol 20:263–274CrossRefPubMedGoogle Scholar
  54. Jentsch JD, Taylor JR (2003) Sex-related differences in spatial divided attention and motor impulsivity in rats. Behav Neurosci 117:76–83CrossRefPubMedGoogle Scholar
  55. Keeler JF, Robbins TW (2011) Translating cognition from animals to humans. Biochem Pharmacol 81:1356–1366CrossRefPubMedGoogle Scholar
  56. Klein LC, Corwin EJ (2002) Seeing the unexpected: how sex differences in stress responses may provide a new perspective on the manifestation of psychiatric disorders. Current Psychiatry Reports 4:441–448CrossRefPubMedGoogle Scholar
  57. Koss WA, Franklin AD, Juraska JM (2011) Delayed alternation in adolescent and adult male and female rats. Dev Psychobiol 53:724–731CrossRefPubMedGoogle Scholar
  58. Le Pen G, Grottick AJ, Higgins GA, Moreau JL (2003) Phencyclidine exacerbates attentional deficits in a neurodevelopmental rat model of schizophrenia. Neuropsychopharmacology 28:1799–1809CrossRefPubMedGoogle Scholar
  59. Lee TY, Kim SN, Jang JH, Shim G, Jung WH, Shin NY, Kwon JS (2013) Neural correlate of impulsivity in subjects at ultra-high risk for psychosis. Prog Neuro-Psychopharmacol Biol Psychiatry 45:165–169CrossRefGoogle Scholar
  60. Lehmann O, Grottick AJ, Cassel JC, Higgins GA (2003) A double dissociation between serial reaction time and radial maze performance in rats subjected to 192 IgG-saporin lesions of the nucleus basalis and/or the septal region. Eur J Neurosci 18:651–666CrossRefPubMedGoogle Scholar
  61. Li HS, Borg E (1991) Age-related loss of auditory sensitivity in two mouse genotypes. Acta Otolaryngol 111:827–834CrossRefPubMedGoogle Scholar
  62. Luck SJ, Ford JM, Sarter M, Lustig C (2012) CNTRICS final biomarker selection: control of attention. Schizophr Bull 38:53–61CrossRefPubMedGoogle Scholar
  63. McGaughy J, Sarter M (1995) Behavioral vigilance in rats: task validation and effects of age, amphetamine, and benzodiazepine receptor ligands. Psychopharmacology 117:340–357CrossRefPubMedGoogle Scholar
  64. Melcher T, Wolter S, Falck S, Wild E, Wild F, Gruber E, Falkai P, Gruber O (2014) Common and disease-specific dysfunctions of brain systems underlying attentional and executive control in schizophrenia and bipolar disorder. Eur Arch Psychiatry Clin Neurosci 264:517–532CrossRefPubMedGoogle Scholar
  65. Millan MJ, Agid Y, Brune M, Bullmore ET, Carter CS, Clayton NS, Connor R, Davis S, Deakin B, DeRubeis RJ, Dubois B, Geyer MA, Goodwin GM, Gorwood P, Jay TM, Joels M, Mansuy IM, Meyer-Lindenberg A, Murphy D, Rolls E, Saletu B, Spedding M, Sweeney J, Whittington M, Young LJ (2012) Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy. Nat Rev Drug Discov 11:141–168CrossRefPubMedGoogle Scholar
  66. Mirsky A, Rosvold H (1960) The use of psychoactive drugs as a neuropsychological tool in studies of attention in man. Drugs and behavior. Wiley, New York, pp 375–392Google Scholar
  67. Moon J, Beaudin AE, Verosky S, Driscoll LL, Weiskopf M, Levitsky DA, Crnic LS, Strupp BJ (2006) Attentional dysfunction, impulsivity, and resistance to change in a mouse model of fragile X syndrome. Behav Neurosci 120:1367–1379CrossRefPubMedGoogle Scholar
  68. Muir JL, Everitt BJ, Robbins TW (1996) The cerebral cortex of the rat and visual attentional function: dissociable effects of mediofrontal, cingulate, anterior dorsolateral, and parietal cortex lesions on a five-choice serial reaction time task. Cereb Cortex 6:470–481CrossRefPubMedGoogle Scholar
  69. Murphy ER, Dalley JW, Robbins TW (2005) Local glutamate receptor antagonism in the rat prefrontal cortex disrupts response inhibition in a visuospatial attentional task. Psychopharmacology 179:99–107CrossRefPubMedGoogle Scholar
  70. Navarra R, Graf R, Huang Y, Logue S, Comery T, Hughes Z, Day M (2008) Effects of atomoxetine and methylphenidate on attention and impulsivity in the 5-choice serial reaction time test. Prog Neuro-Psychopharmacol Biol Psychiatry 32:34–41CrossRefGoogle Scholar
  71. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161–1169CrossRefPubMedPubMedCentralGoogle Scholar
  72. Nuechterlein KH, Green MF, Kern RS, Baade LE, Barch DM, Cohen JD, Essock S, Fenton WS, Frese FJ 3rd, Gold JM, Goldberg T, Heaton RK, Keefe RS, Kraemer H, Mesholam-Gately R, Seidman LJ, Stover E, Weinberger DR, Young AS, Zalcman S, Marder SR (2008) The MATRICS Consensus Cognitive Battery, part 1: test selection, reliability, and validity. Am J Psychiatry 165:203–213CrossRefPubMedGoogle Scholar
  73. Nuechterlein KH, Luck SJ, Lustig C, Sarter M (2009) CNTRICS final task selection: control of attention. Schizophr Bull 35:182–196CrossRefPubMedPubMedCentralGoogle Scholar
  74. Oltmanns TF (1978) Selective attention in schizophrenic and manic psychoses: the effect of distraction on information processing. J Abnorm Psychol 87:212–225CrossRefPubMedGoogle Scholar
  75. Oltmanns TF, Neale JM (1975) Schizophrenic performance when distractors are present: attentional deficit or differential task difficulty? J Abnorm Psychol 84:205–209CrossRefPubMedGoogle Scholar
  76. Ouzir M (2013) Impulsivity in schizophrenia: a comprehensive update. Aggress Violent Behav 18:247–254CrossRefGoogle Scholar
  77. Paine TA, Carlezon WA Jr (2009) Effects of antipsychotic drugs on MK-801-induced attentional and motivational deficits in rats. Neuropharmacology 56:788–797CrossRefPubMedPubMedCentralGoogle Scholar
  78. Papaleo F, Erickson L, Liu G, Chen J, Weinberger DR (2012) Effects of sex and COMT genotype on environmentally modulated cognitive control in mice. Proc Natl Acad Sci U S A 109:20160–20165CrossRefPubMedPubMedCentralGoogle Scholar
  79. Patel S, Stolerman IP, Asherson P, Sluyter F (2006) Attentional performance of C57BL/6 and DBA/2 mice in the 5-choice serial reaction time task. Behav Brain Res 170:197–203CrossRefPubMedGoogle Scholar
  80. Reddy LF, Lee J, Davis MC, Altshuler L, Glahn DC, Miklowitz DJ, Green MF (2014) Impulsivity and risk taking in bipolar disorder and schizophrenia. Neuropsychopharmacology 39:456–463CrossRefPubMedGoogle Scholar
  81. Robbins TW (2002) The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology 163:362–380CrossRefPubMedGoogle Scholar
  82. Robbins TW, Gillan CM, Smith DG, de Wit S, Ersche KD (2012) Neurocognitive endophenotypes of impulsivity and compulsivity: towards dimensional psychiatry. Trends Cogn Sci 16:81–91CrossRefPubMedGoogle Scholar
  83. Sannino S, Gozzi A, Cerasa A, Piras F, Scheggia D, Manago F, Damiano M, Galbusera A, Erickson LC, De Pietri TD, Bifone A, Tsaftaris SA, Caltagirone C, Weinberger DR, Spalletta G, Papaleo F (2015) COMT genetic reduction produces sexually divergent effects on cortical anatomy and working memory in mice and humans. Cereb Cortex 25:2529–2541CrossRefPubMedGoogle Scholar
  84. Sarter M, Bruno JP, Givens B, Moore H, McGaughy J, McMahon K (1996) Neuronal mechanisms mediating drug-induced cognition enhancement: cognitive activity as a necessary intervening variable. Brain Res Cogn Brain Res 3:329–343CrossRefPubMedGoogle Scholar
  85. Sharma T, Antonova L (2003) Cognitive function in schizophrenia. Deficits, functional consequences, and future treatment. Psychiatr Clin North Am 26:25–40CrossRefPubMedGoogle Scholar
  86. Smid HG, Martens S, de Witte MR, Bruggeman R (2013) Inflexible minds: impaired attention switching in recent-onset schizophrenia. PLoS One 8(10):e78062. doi:10.1371/journal.pone.0078062
  87. St Peters M, Cherian AK, Bradshaw M, Sarter M (2011) Sustained attention in mice: expanding the translational utility of the SAT by incorporating the Michigan Controlled Access Response Port (MICARP). Behav Brain Res 225:574–583CrossRefPubMedPubMedCentralGoogle Scholar
  88. Stangle DE, Smith DR, Beaudin SA, Strawderman MS, Levitsky DA, Strupp BJ (2007) Succimer chelation improves learning, attention, and arousal regulation in lead-exposed rats but produces lasting cognitive impairment in the absence of lead exposure. Environ Health Perspect 115:201–209CrossRefPubMedGoogle Scholar
  89. Sumich A, Castro A, Anilkumar AP, Zachariah E, Kumari V (2013) Neurophysiological correlates of excitement in schizophrenia. Prog Neuro-Psychopharmacol Biol Psychiatry 46:132–138CrossRefGoogle Scholar
  90. Voon V, Irvine MA, Derbyshire K, Worbe Y, Lange I, Abbott S, Morein-Zamir S, Dudley R, Caprioli D, Harrison NA, Wood J, Dalley JW, Bullmore ET, Grant JE, Robbins TW (2014) Measuring “waiting” impulsivity in substance addictions and binge eating disorder in a novel analogue of rodent serial reaction time task. Biol Psychiatry 75:148–155CrossRefPubMedPubMedCentralGoogle Scholar
  91. Walitza S, Melfsen S, Herhaus G, Scheuerpflug P, Warnke A, Muller T, Lange KW, Gerlach M (2007) Association of Parkinson’s disease with symptoms of attention deficit hyperactivity disorder in childhood. J Neural Transm Suppl 72:311–315CrossRefGoogle Scholar
  92. Werling DM, Geschwind DH (2013) Sex differences in autism spectrum disorders. Curr Opin Neurol 26:146–153CrossRefPubMedPubMedCentralGoogle Scholar
  93. Willott JF, Bross LS (1996) Morphological changes in the anteroventral cochlear nucleus that accompany sensorineural hearing loss in DBA/2J and C57BL/6J mice. Brain Res Dev Brain Res 91:218–226CrossRefPubMedGoogle Scholar
  94. Wrenn CC, Turchi JN, Schlosser S, Dreiling JL, Stephenson DA, Crawley JN (2006) Performance of galanin transgenic mice in the 5-choice serial reaction time attentional task. Pharmacol Biochem Behav 83:428–440CrossRefPubMedGoogle Scholar
  95. Young JW, Jentsch JD, Bussey TJ, Wallace TL, Hutcheson DM (2013) Consideration of species differences in developing novel molecules as cognition enhancers. Neurosci Biobehav Rev 37:2181–2193CrossRefPubMedGoogle Scholar
  96. Zvyagintsev M, Parisi C, Chechko N, Nikolaev AR, Mathiak K (2013) Attention and multisensory integration of emotions in schizophrenia. Front Hum Neurosci 7:674. doi:10.3389/fnhum.2013.00674

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Huiping Huang
    • 1
  • Simone Guadagna
    • 1
  • Maddalena Mereu
    • 2
  • Mariasole Ciampoli
    • 1
  • Giacomo Pruzzo
    • 1
  • Theresa Ballard
    • 3
  • Francesco Papaleo
    • 1
  1. 1.Department of Neuroscience and Brain TechnologiesIstituto Italiano di TecnologiaGenovaItaly
  2. 2.Dipartimento di Scienze del FarmacoUniversità degli Studi di PadovaPadovaItaly
  3. 3.Neuroscience, Ophthalmology and Rare Diseases, Roche Pharma Research and Early DevelopmentRoche Innovation CenterBaselSwitzerland

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