Long term compulsivity on the 5-choice serial reaction time task after acute Chlorpyrifos exposure

Toxicology Letters

Volumn 216, Issue 2-3, 2013, Pages 73-85

  Montes de Oca, Lara ^a   Moreno, Margarita ^a   Cardona, Diana ^a   Campa, Leticia ^b   Suñol, Cristina ^b   Galofré, Mireia ^b   Flores, Pilar ^a   Sánchez Santed, Fernando ^a  

^a UNIVERSITY OF ALMERÍA   (Spain)

^b INST D INVESTIGACIONS B   (Spain)

Author keywords

Compulsivity; D Amphetamine; Five choice serial reaction time task; Neurotoxicity; Neurotransmitter; Pesticides

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; AMPHETAMINE; CHLORPYRIFOS; DIZOCILPINE; GLUTAMIC ACID; KETANSERIN; MONOAMINE; PRESERVATIVE; QUINPIROLE;

5 CHOICE SERIAL REACTION TIME TASK; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; BRAIN REGION; COMPULSION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE METABOLISM; HIPPOCAMPUS; MALE; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; RAT; REACTION TIME;

ANIMALS; BIOGENIC MONOAMINES; BRAIN; CHLORPYRIFOS; CHOLINESTERASE INHIBITORS; COMPULSIVE BEHAVIOR; DEXTROAMPHETAMINE; GAMMA-AMINOBUTYRIC ACID; MALE; RANDOM ALLOCATION; RATS; REACTION TIME;

RATTUS;

EID: 84871552907     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.11.012     Document Type: Article

References (81)

1. Aldridge J.E., Meyer A., Seidler F.J., Slotkin T.A. Alterations in central nervous system serotonergic and dopaminergic synaptic activity in adulthood after prenatal or neonatal chlorpyrifos exposure. Environmental Health Perspectives 2005, 113:1027-1031.
2. Asanuma M., Miyazaki I., Diaz-Corrales F.J., Ogawa N. Quinone formation as dopaminergic neuron-specific oxidative stress in the pathogenesis of sporadic Parkinson's disease and neurotoxin-induced parkinsonism. Acta Medica Okayama 2004, 58:221-233.
3. Bari A., Dalley J.W., Robbins T.W. The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nature Protocols 2008, 3:759-767.
4. Baunez C., Robbins T.W. Effects of dopamine depletion of the dorsal striatum and further interaction with subthalamic nucleus lesions in an attentional task in the rat. Neuroscience 1999, 92:1343-1356.
5. Bhagat Y.A., Obenaus A., Hamilton M.G., Kendall E.J. Magnetic resonance imaging predicts neuropathology from soman-mediated seizures in the rodent. Neuroreport 2001, 12:1481-1487.
6. Bhagat Y.A., Obenaus A., Hamilton M.G., Mikler J., Kendall E.J. Neuroprotection from soman-induced seizures in the rodent: evaluation with diffusion- and T2-weighted magnetic resonance imaging. Neurotoxicology 2005, 26:1001-1013.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
8. Brown T.P., Rumsby P.C., Capleton A.C., Rushton L., Levy L.S. Pesticides and Parkinson's disease - is there a link?. Environmental Health Perspectives 2006, 114:156-164.
9. Cardona D., Lopez Grancha M., Lopez Crespo G., Nieto Escamez F., Sanchez Santed F., Flores P. Vulnerability of long-term neurotoxicity of chlorpyrifos: effect on schedule-induced polydipsia and a delay discounting task. Psychopharmacology (Berlin) 2006, 189:47-57.
10. Cardona D., Lopez-Crespo G., Sanchez-Amate M.C., Flores P., Sanchez-Santed F. Impulsivity as long-term sequelae after chlorpyrifos intoxication: time course and individual differences. Neurotoxicity Research 2011, 19:128-137.
11. Carli M., Baviera M., Invernizzi R.W., Balducci C. Dissociable contribution of 5-HT1A and 5-HT2A receptors in the medial prefrontal cortex to different aspects of executive control such as impulsivity and compulsive perseveration in rats. Neuropsychopharmacology 2006, 31:757-767.
12. Carli M., Calcagno E., Mainini E., Arnt J., Invernizzi R.W. Sertindole restores attentional performance and suppresses glutamate release induced by the NMDA receptor antagonist CPP. Psychopharmacology (Berlin) 2011, 214:625-637.
13. Carli M., Calcagno E., Mainolfi P., Mainini E., Invernizzi R.W. 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 (Berlin) 2011, 214:639-652.
14. Carli M., Robbins T.W., Evenden J.L., Everitt B.J. 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. Behavioural Brain Research 1983, 9:361-380.
15. Casida J.E., Quistad G.B. Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets. Chemical Research in Toxicology 2004, 17:983-998.
16. Chamberlain S.R., Blackwell A.D., Fineberg N.A., Robbins T.W., Sahakian B.J. The neuropsychology of obsessive compulsive disorder: the importance of failures in cognitive and behavioural inhibition as candidate endophenotypic markers. Neuroscience & Biobehavioral Reviews 2005, 29:399-419.
17. Chamberlain S.R., Menzies L., Hampshire A., Suckling J., Fineberg N.A., del Campo N., Aitken M., Craig K., Owen A.M., Bullmore E.T., Robbins T.W., Sahakian B.J. Orbitofrontal dysfunction in patients with obsessive-compulsive disorder and their unaffected relatives. Science 2008, 321:421-422.
18. Chao L.L., Rothlind J.C., Cardenas V.A., Meyerhoff D.J., Weiner M.W. Effects of low-level exposure to sarin and cyclosarin during the 1991 Gulf War on brain function and brain structure in US veterans. Neurotoxicology 2010, 31:493-501.
19. Chudasama Y., Baunez C., Robbins T.W. Functional disconnection of the medial prefrontal cortex and subthalamic nucleus in attentional performance: evidence for corticosubthalamic interaction. Journal of Neuroscience 2003, 23:5477-5485.
20. Chudasama Y., Passetti F., Rhodes S.E.V., Lopian D., Desai A., Robbins T.W. 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. Behavioural Brain Research 2003, 146:105-119.
21. Cole B.J., Robbins T.W. Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: implications for theories of selective attention and arousal. Behavioural Brain Research 1989, 33:165-179.
22. Cools R., Barker R.A., Sahakian B.J., Robbins T.W. l-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson's disease. Neuropsychologia 2003, 41:1431-1441.
23. Crider A. Perseveration in schizophrenia. Schizophrenia Bulletin 1997, 23:63-74.
24. Dalley J.W., Everitt B.J., Robbins T.W. Impulsivity, compulsivity, and top-down cognitive control. Neuron 2011, 69:680-694.
25. Dalley J.W., Mar A.C., Economidou D., Robbins T.W. Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional neurochemistry. Pharmacology Biochemistry and Behavior 2008, 90:250-260.
26. Day M., Balci F., Wan H.I., Fox G.B., Rutkowski J.L., Feuerstein G. Cognitive endpoints as disease biomarkers: optimizing the congruency of preclinical models to the clinic. Current Opinion in Investigational Drugs 2008, 9:696-706.
27. Del Arco A., Castaneda T.R., Mora F. Amphetamine releases GABA in striatum of the freely moving rat: involvement of calcium and high affinity transporter mechanisms. Neuropharmacology 1998, 37:199-205.
28. Del Arco A., Gonzalez-Mora J.L., Armas V.R., Mora F. Amphetamine increases the extracellular concentration of glutamate in striatum of the awake rat: involvement of high affinity transporter mechanisms. Neuropharmacology 1999, 38:943-954.
29. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 1961, 7:88-90.
30. Fineberg N.A., Potenza M.N., Chamberlain S.R., Berlin H.A., Menzies L., Bechara A., Sahakian B.J., Robbins T.W., Bullmore E.T., Hollander E. Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology 2010, 35:591-604.
31. Gescheidt T., Bares M. Impulse control disorders in patients with Parkinson's disease. Acta Neurologica Belgica 2011, 111:3-9.
32. Golomb B.A. Acetylcholinesterase inhibitors and Gulf War illnesses. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:4295-4300.
33. Halliwell B. Oxidative stress and neurodegeneration: where are we now?. Journal of Neurochemistry 2006, 97:1634-1658.
34. Hayden K.M., Norton M.C., Darcey D., Ostbye T., Zandi P.P., Breitner J.C., Welsh-Bohmer K.A. Occupational exposure to pesticides increases the risk of incident AD: the Cache County study. Neurology 2010, 74:1524-1530. Cache County Study Investigators.
35. Higgins G.A., Enderlin M., Haman M., Fletcher P.J. The 5-HT2A receptor antagonist M100,907 attenuates motor and 'impulsive-type' behaviours produced by NMDA receptor antagonism. Psychopharmacology (Berlin) 2003, 170:309-319.
36. Hoyle E., Genn R.F., Fernandes C., Stolerman I.P. Impaired performance of alpha7 nicotinic receptor knockout mice in the five-choice serial reaction time task. Psychopharmacology (Berlin) 2006, 189:211-223.
37. Hsieh B.H., Deng J.F., Ger J., Tsai W.J. Acetylcholinesterase inhibition and the extrapyramidal syndrome: a review of the neurotoxicity of organophosphate. Neurotoxicology 2001, 22:423-427.
38. Jenner P. Oxidative stress in Parkinson's disease. Annals of Neurology 2003, 53(Suppl. 3):S26-36. discussion S36-S38.
39. Karen D.J., Li W., Harp P.R., Gillette J.S., Bloomquist J.R. Striatal dopaminergic pathways as a target for the insecticides permethrin and chlorpyrifos. Neurotoxicology 2001, 22:811-817.
40. Keenan K.P., Ballam G.C., Haught D.G., Laroque P. Nutrition. The Laboratory Rat 2000, 57-75. Academic Press, London. G.J. Krinke (Ed.).
41. Li Z., Liang Y., Boules M., Gordillo A., Richelson E. Effect of amphetamine on extracellular concentrations of amino acids in striatum in neurotensin subtype 1 and 2 receptor null mice: a possible interaction between neurotensin receptors and amino acid systems for study of schizophrenia. Neuropharmacology 2010, 58:1174-1178.
42. London L., Flisher A.J., Wesseling C., Mergler D., Kromhout H. Suicide and exposure to organophosphate insecticides: cause or effect?. American Journal of Industrial Medicine 2005, 47:308-321.
43. Lotti M. Clinical Toxicology of Anticholinesterase Agents in Humans. Handbook of Pesticide Toxicology 2001, 1043-1085. Academic Press, San Diego. R.I. Krieger, W.C. Krieger (Eds.).
44. Mackenzie Ross S.J., Brewin C.R., Curran H.V., Furlong C.E., Abraham-Smith K.M., Harrison V. Neuropsychological and psychiatric functioning in sheep farmers exposed to low levels of organophosphate pesticides. Neurotoxicology and Teratology 2010, 32:452-459.
45. Middlemore-Risher M.L., Buccafusco J.J., Terry J.A.V. Repeated exposures to low-level chlorpyrifos results in impairments in sustained attention and increased impulsivity in rats. Neurotoxicology and Teratology 2010, 32:415-424.
46. Mijatovic J., Piltonen M., Alberton P., Männistö P.T., Saarma M., Piepponen T.P. Constitutive Ret signaling is protective for dopaminergic cell bodies but not for axonal terminals. Neurobiology of Aging 2011, 32:1486-1494.
47. Moreno M., Cardona D., Gomez M.J., Sanchez-Santed F., Tobena A., Fernandez-Teruel A., Campa L., Sunol C., Escarabajal M.D., Torres C., Flores P. Impulsivity characterization in the Roman high- and low-avoidance rat strains: behavioral and neurochemical differences. Neuropsychopharmacology 2010, 35:1198-1208.
48. Moreno M., Flores P. Schedule-induced polydipsia as a model of compulsive behavior: neuropharmacological and neuroendocrine bases. Psychopharmacology (BerlIN) 2012, 219:647-659.
49. Moreno M., Cañadas F., Cardona D., Suñol C., Campa L., Sánchez-Amate M.C., Flores P., Sanchez-Santed F. Long-term monoamine changes in the striatum and nucleus accumbens after acute chlorpyrifos exposure. Toxicology Letters 2008, 176:162-167.
50. Moser V.C. Comparisons of the acute effects of cholinesterase inhibitors using a neurobehavioral screening battery in rats. Neurotoxicology and Teratology 1995, 17:617-625.
51. Muir J.L., Everitt B.J., Robbins T.W. 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. Cerebral Cortex 1996, 6:470-481.
52. Murphy E.R., Robinson E.S., Theobald D.E., Dalley J.W., Robbins T.W. Contrasting effects of selective lesions of nucleus accumbens core or shell on inhibitory control and amphetamine-induced impulsive behaviour. European Journal of Neurology 2008, 28:353-363.
53. Nomura D.K., Casida J.E. Activity-based protein profiling of organophosphorus and thiocarbamate pesticides reveals multiple serine hydrolase targets in mouse brain. Journal of Agricultural and Food Chemistry 2011, 59:2808-2815.
54. Paine T.A., Tomasiewicz H.C., Zhang K., Carlezon W.A. Sensitivity of the five-choice serial reaction time task to the effects of various psychotropic drugs in Sprague-Dawley rats. Biological Psychiatry 2007, 62:687-693.
55. Parron T., Requena M., Hernandez A.F., Alarcon R. Association between environmental exposure to pesticides and neurodegenerative diseases. Toxicology and Applied Pharmacology 2011, 256:379-385.
56. Passetti F., Dalley J.W., Robbins T.W. Double dissociation of serotonergic and dopaminergic mechanisms on attentional performance using a rodent five-choice reaction time task. Psychopharmacology (Berlin) 2003, 165:136-145.
57. Paterson N.E., Ricciardi J., Wetzler C., Hanania T. Sub-optimal performance in the 5-choice serial reaction time task in rats was sensitive to methylphenidate, atomoxetine and d-amphetamine, but unaffected by the COMT inhibitor tolcapone. Neuroscience Research 2011, 69:41-50.
58. Perry J.L., Stairs D.J., Bardo M.T. Impulsive choice and environmental enrichment: effects of d-amphetamine and methylphenidate. Behavioural Brain Research 2008, 193:48-54.
59. Pezze M.A., Dalley J.W., Robbins T.W. Differential roles of dopamine D1 and D2 receptors in the nucleus accumbens in attentional performance on the five-choice serial reaction time task. Neuropsychopharmacology 2007, 32:273-283.
60. Ponsen M.M., Stoffers D., Twisk J.W., Wolters E.C., Berendse H.W. Hyposmia and executive dysfunction as predictors of future Parkinson's disease: a prospective study. Movement Disorders 2009, 24:1060-1065.
61. Pope C.N., Chakraborti T.K., Chapman M.L., Farrar J.D. Long-term neurochemical and behavioral effects induced by acute chlorpyrifos treatment. Pharmacology Biochemistry and Behavior 1992, 42:251-256.
62. Robbins T.W. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berlin) 2002, 163:362-380.
63. Robert G., Drapier D., Verin M., Millet B., Azulay J.P., Blin O. Cognitive impulsivity in Parkinson's disease patients: assessment and pathophysiology. Movement Disorders 2009, 24:2316-2327.
64. Rochat L., Delbeuck X., Billieux J., d'Acremont M., Van der Linden A.C., Van der Linden M. Assessing impulsivity changes in Alzheimer disease. Alzheimer Disease and Associated Disorders 2008, 22:278-283.
65. Roldan-Tapia L., Nieto-Escamez F.A., del Aguila E.M., Laynez F., Parron T., Sanchez-Santed F. Neuropsychological sequelae from acute poisoning and long-term exposure to carbamate and organophosphate pesticides. Neurotoxicology and Teratology 2006, 28:694-703.
66. Roldán-Tapia L., Parrón T., Sánchez-Santed F. Neuropsychological effects of long-term exposure to organophosphate pesticides. Neurotoxicology and Teratology 2005, 27:259-266.
67. Ruiz-Muñoz A.M., Nieto-Escamez F.A., Aznar S., Colomina M.T., Sanchez-Santed F. Cognitive and histological disturbances after chlorpyrifos exposure and chronic Aβ(1-42) infusions in Wistar rats. Neurotoxicology 2011, 32:836-844.
68. Salazar J.G., Ribes D., Cabre M., Domingo J.L., Sanchez-Santed F., Colomina M.T. Amyloid beta peptide levels increase in brain of AbetaPP Swedish mice after exposure to chlorpyrifos. Current Alzheimer Research 2011, 8:732-740.
69. Salvi R.M., Lara D.R., Ghisolfi E.S., Portela L.V., Dias R.D., Souza D.O. Neuropsychiatric evaluation in subjects chronically exposed to organophosphate pesticides. Toxicological Sciences 2003, 72:267-271.
70. Sánchez-Santed F., Cañadas F., Flores P., López-Grancha M., Cardona D. Long-term functional neurotoxicity of paraoxon and chlorpyrifos: behavioural and pharmacological evidence. Neurotoxicology and Teratology 2004, 26:305-317.
71. Santibanez M., Bolumar F., Garcia A.M. Occupational risk factors in Alzheimer's disease: a review assessing the quality of published epidemiological studies. Occupational and Environmental Medicine 2007, 64:723-732.
72. Stoffers D., Berendse H.W., Deijen J.B., Wolters E.C. Motor perseveration is an early sign of Parkinson's disease. Neurology 2001, 57:2111-2113.
73. Terry A.V., Gearhart D.A., Beck W.D., Truan J.N., Middlemore M.L., Williamson L.N., Bartlett M.G., Prendergast M.A., Sickles D.W., Buccafusco J.J. Chronic, intermittent exposure to chlorpyrifos in rats: protracted effects on axonal transport, neurotrophin receptors, cholinergic markers, and information processing. Journal of Pharmacology and Experimental Therapeutics 2007, 322:1117-1128.
74. Testai E., Buratti F.M., Di Consiglio E. Chlorpyrifos. Hayes' Handbook of Pesticide Toxicology 2010, 1505-1526. Academic Press, New York. R. Krieger (Ed.).
75. Torres-Altoro M.I., Mathur B.N., Drerup J.M., Thomas R., Lovinger D.M., O'Callaghan J.P., Bibb J.A. Organophosphates dysregulate dopamine signaling, glutamatergic neurotransmission, and induce neuronal injury markers in striatum. Journal of Neurochemistry 2011, 119:303-313.
76. van Gaalen M.M., Brueggeman R.J., Bronius P.F., Schoffelmeer A.N., Vanderschuren L.J. Behavioral disinhibition requires dopamine receptor activation. Psychopharmacology (Berlin) 2006, 187:73-85.
77. Wesseling C., van Wendel de Joode B., Keifer M., London L., Mergler D., Stallones L. Symptoms of psychological distress and suicidal ideation among banana workers with a history of poisoning by organophosphate or n-methyl carbamate pesticides. Occupational and Environmental Medicine 2010, 67:778-784.
78. Winstanley C.A., Eagle D.M., Robbins T.W. Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clinical Psychology Review 2006, 26:379-395.
79. Winstanley C.A., Zeeb F.D., Bedard A., Fu K., Lai B., Steele C., Wong A.C. Dopaminergic modulation of the orbitofrontal cortex affects attention, motivation and impulsive responding in rats performing the five-choice serial reaction time task. Behavioural Brain Research 2010, 210:263-272.
80. Yamasue H., Abe O., Kasai K., Suga M., Iwanami A., Yamada H., Tochigi M., Ohtani T., Rogers M.A., Sasaki T., Aoki S., Kato T., Kato N. Human brain structural change related to acute single exposure to sarin. Annals of Neurology 2007, 61:37-46.
81. Zaja-Milatovic S., Gupta R.C., Aschner M., Milatovic D. Protection of DFP-induced oxidative damage and neurodegeneration by antioxidants and NMDA receptor antagonist. Toxicology and Applied Pharmacology 2009, 240:124-131.