Measuring behaviour in rodents: Towards translational neuropsychiatric research

Behavioural Brain Research

Volumn 236, Issue 1, 2013, Pages 295-306

  Homberg, Judith R ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

Author keywords

Activation; Behaviour; Construct validity; Endophenotype; Motivation; Perception; Switching; Task; Translational

Indexed keywords

ANIMAL BEHAVIOR; BEHAVIOR CHANGE; BRAIN REGION; CONSTRUCT VALIDITY; DISEASE ASSOCIATION; ENDOPHENOTYPE; ENVIRONMENTAL FACTOR; FACE VALIDITY; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; INSTRUMENTAL CONDITIONING; MENTAL DISEASE; MOLECULAR DYNAMICS; MOTIVATION; NEUROPSYCHIATRY; NONHUMAN; PATHOPHYSIOLOGY; PERCEPTION; PREDICTIVE VALIDITY; PRIORITY JOURNAL; REVIEW; SELECTIVE ATTENTION; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; TASK PERFORMANCE; TRANSLATIONAL RESEARCH; VISUAL STIMULATION;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; GENE-ENVIRONMENT INTERACTION; MENTAL DISORDERS; MICE; MOTIVATION; PERCEPTION; PHENOTYPE; PSYCHOLOGY, EXPERIMENTAL; PSYCHOMOTOR PERFORMANCE; RATS; REPRODUCIBILITY OF RESULTS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84866540307     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.09.005     Document Type: Review

References (138)

1. van Os J., Rutten B.P., Poulton R. Gene-environment interactions in schizophrenia: review of epidemiological findings and future directions. Schizophrenia Bulletin 2008, 34:1066-1082.
2. Bearden C.E., Freimer N.B. Endophenotypes for psychiatric disorders: ready for primetime?. Trends in Genetics 2006, 22:3066-3313.
3. Jaffee S.R., Price T.S. Gene-environment correlations: a review of the evidence and implications for prevention of mental illness. Molecular Psychiatry 2007, 12:432-442.
4. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
5. Hasler G., Drevets W.C., Manji H.K., Charney D.S. Discovering endophenotypes for major depression. Neuropsychopharmacology 2004, 29:1765-1781.
6. Mitchell C., Notterman D., Brooks-Gunn J., Hobcraft J., Garfinkel I., Jaeger K., et al. Role of mother's genes and environment in postpartum depression. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:8189-8193.
7. Belsky J., Jonassaint C., Pluess M., Stanton M., Brummett B., Williams R. Vulnerability genes or plasticity genes?. Molecular Psychiatry 2009, 14:746-754.
8. Homberg J.R., Lesch K.P. Looking on the bright side of serotonin transporter gene variation. Biological Psychiatry 2010, 69:513-519.
9. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. European Journal of Pharmacology 1978, 47:379-391.
10. Kalueff A.V., Olivier J.D., Nonkes L.J., Homberg J.R. Conserved role for the serotonin transporter gene in rat and mouse neurobehavioral endophenotypes. Neuroscience and Biobehavioral Reviews 2010, 34:373-386.
11. Nonkes L.J., Maes J.H., Homberg J.R. Improved cognitive flexibility in serotonin transporter knockout rats is unchanged following chronic cocaine self-administration. Addiction Biology 2011, 10.1111/j.1369-1600.2011.00351.x.
12. Brigman J.L., Mathur P., Harvey-White J., Izquierdo A., Saksida L.M., Bussey T.J., et al. Pharmacological or genetic inactivation of the serotonin transporter improves reversal learning in mice. Cerebral Cortex 2010, 20:1955-1963.
13. Waikar S.V., Craske M.G. Cognitive correlates of anxious and depressive symptomatology: an examination of the Helplessness/Hopelessness model. Journal of Anxiety Disorders 1997, 11(January-February (1)):1-16.
14. Remijnse P.L., Nielen M.M., van Balkom A.J., Hendriks G.J., Hoogendijk W.J., Uylings H.B., et al. Differential frontal-striatal and paralimbic activity during reversal learning in major depressive disorder and obsessive-compulsive disorder. Psychological Medicine 2009, 39:1503-1518.
15. Nonkes L.J., Tomson K., Maertin A., Dederen J., Roald Maes J.H., Homberg J. Orbitofrontal cortex and amygdalar over-activity is associated with an inability to use the value of expected outcomes to guide behaviour in serotonin transporter knockout rats. Neurobiology of Learning and Memory 2010, 94:65-72.
16. Nonkes L.J., van de Vondervoort I.I., de Leeuw M.J., Wijlaars L.P., Maes J.H., Homberg J.R. Serotonin transporter knockout rats show improved strategy set-shifting and reduced latent inhibition. Learning and Memory 2012, 19:190-193.
17. Nonkes L.J., de Pooter M., Homberg J.R. Behavioural therapy based on distraction alleviates impaired fear extinction in male serotonin transporter knockout rats. Journal of Psychiatry and Neuroscience 2012, 37:224-230.
18. Markou A., Chiamulera C., Geyer M.A., Tricklebank M., Steckler T. Removing obstacles in neuroscience drug discovery: the future path for animal models. Neuropsychopharmacology 2009, 34:74-89.
19. Willner P. The validity of animal models of depression. Psychopharmacology 1984, 83:1-16.
20. Boulougouris V., Chamberlain S.R., Robbins T.W. Cross-species models of OCD spectrum disorders. Psychiatry Research 2009, 170:15-21.
21. Fineberg N., Chamberlain S., Hollander E., Boulougouris V., Robbins T. Translational approaches to obsessive compulsive disorder from animal models to clinical treatment. British Journal of Pharmacology 2011, 164:1044-1061.
22. Danet M., Lapiz-Bluhm S., Morilak D.A. A cognitive deficit induced in rats by chronic intermittent cold stress is reversed by chronic antidepressant treatment. International Journal of Neuropsychopharmacology 2010, 13:997-1009.
23. Dickstein D.P., Finger E.C., Skup M., Pine D.S., Blair J.R., Leibenluft E. Altered neural function in pediatric bipolar disorder during reversal learning. Bipolar Disorders 2010, 12:707-719.
24. Calu D.J., Stalnaker T.A., Franz T.M., Singh T., Shaham Y., Schoenbaum G. Withdrawal from cocaine self-administration produces long-lasting deficits in orbitofrontal-dependent reversal learning in rats. Learning and Memory 2007, 14:325-328.
25. Ersche K.D., Roiser J.P., Robbins T.W., Sahakian B.J. Chronic cocaine but not chronic amphetamine use is associated with perseverative responding in humans. Psychopharmacology 2008, 197:421-431.
26. Budhani S., Richell R.A., Blair R.J. Impaired reversal but intact acquisition: probabilistic response reversal deficits in adult individuals with psychopathy. Journal of Abnormal Psychology 2006, 115:552-558.
27. Cryan J.F., Markou A., Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends in Pharmacological Sciences 2002, 23:238-245.
28. Rupniak N.M. Animal models of depression: challenges from a drug development perspective. Behavioural Pharmacology 2003, 14:385-390.
29. Cryan J.F., Valentino R.J., Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neuroscience and Biobehavioral Reviews 2005, 29:547-569.
30. Floresco S.B., Geyer M.A., Gold L.H., Grace A.A. Developing predictive animal models and establishing a preclinical trials network for assessing treatment effects on cognition in schizophrenia. Schizophrenia Bulletin 2005, 31:888-894.
31. Geyer M.A., Heinssen R. New approaches to measurement and treatment research to improve cognition in schizophrenia. Schizophrenia Bulletin 2005, 31:806-809.
32. Premack D. Human and animal cognition: continuity and discontinuity. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:13861-13867.
33. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nature Neuroscience 2010, 13:1161-1169.
34. Keeler J.F., Robbins T.W. Translating cognition from animals to humans. Biochemical Pharmacology 2011, 81:1356-1366.
35. Bouton M.E. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biological Psychiatry 2002, 52:976-986.
36. Markram K., Rinaldi T., La M.D., Sandi C., Markram H. Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 2008, 33:901-912.
37. Peters J., Kalivas P.W., Quirk G.J. Extinction circuits for fear and addiction overlap in prefrontal cortex. Learning and Memory 2009, 16:279-288.
38. Milad M.R., Pitman R.K., Ellis C.B., Gold A.L., Shin L.M., Lasko N.B., et al. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry 2009, 66:1075-1082.
39. Milad M.R., Rauch S.L., Pitman R.K., Quirk G.J. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biological Psychology 2006, 73:61-71.
40. Amat J., Baratta M.V., Paul E., Bland S.T., Watkins L.R., Maier S.F. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neuroscience 2005, 8:365-371.
41. Eshel N., Roiser J.P. Reward and punishment processing in depression. Biological Psychiatry 2010, 68:118-124.
42. Murray E.A., Wise S.P., Drevets W.C. Localization of dysfunction in major depressive disorder: prefrontal cortex and amygdala. Biological Psychiatry 2011, 69:e43-e54.
43. Gottesman I.I., Shields J. Genetic theorizing and schizophrenia. British Journal of Psychiatry 1973, 122:15-30.
44. Chamberlain S.R., Menzies L., Hampshire A., Suckling J., Fineberg N.A., del C.N., et al. Orbitofrontal dysfunction in patients with obsessive-compulsive disorder and their unaffected relatives. Science 2008, 321:421-422.
45. Gould T.D., Gottesman I.I. Neuropsychiatric endophenotypes and the development of valid animal models. Genes, Brain, and Behavior 2006, 5:113-119.
46. Hyman S.E., Fenton W.S. Medicine. What are the right targets for psychopharmacology?. Science 2003, 299:350-351.
47. Fernando A.B., Robbins T.W. Animal models of neuropsychiatric disorders. Annual Review of Clinical Psychology 2010, 7:39-61.
48. Hasler G., Drevets W.C., Gould T.D., Gottesman I.I., Manji H.K. Toward constructing an endophenotype strategy for bipolar disorders. Biological Psychiatry 2006, 60:93-105.
49. Einat H. Modelling facets of mania - new directions related to the notion of endophenotypes. Journal of Psychopharmacology 2006, 20:714-722.
50. Amann L.C., Gandal M.J., Halene T.B., Ehrlichman R.S., White S.L., McCarren H.S., et al. Mouse behavioral endophenotypes for schizophrenia. Brain Research Bulletin 2010, 83:147-161.
51. Kellendonk C., Simpson E.H., Kandel E.R. Modeling cognitive endophenotypes of schizophrenia in mice. Trends in Neurosciences 2009, 32:347-358.
52. Allen A.J., Griss M.E., Folley B.S., Hawkins K.A., Pearlson G.D. Endophenotypes in schizophrenia: a selective review. Schizophrenia Research 2009, 109:24-37.
53. Robbins T.W., Gillan C.M., Smith D.G., de Wit S., Ersche K.D. Neurocognitive endophenotypes of impulsivity and compulsivity: towards dimensional psychiatry. Trends in Cognitive Sciences 2012, 16:81-91.
54. Cools R., Nakamura K., Daw N.D. Serotonin and dopamine: unifying affective, activational, and decision functions. Neuropsychopharmacology 2011, 36:98-113.
55. Samochowiec J., Rybakowski F., Czerski P., Zakrzewska M., Stepien G., Pelka-Wysiecka J., et al. Polymorphisms in the dopamine, serotonin, and norepinephrine transporter genes and their relationship to temperamental dimensions measured by the Temperament and Character Inventory in healthy volunteers. Neuropsychobiology 2001, 43:248-253.
56. Jedema H.P., Gianaros P.J., Greer P.J., Kerr D.D., Liu S., Higley J.D., et al. Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. Molecular Psychiatry 2010, 15:512-522. 446.
57. Garcia-Garcia M., Barcelo F., Clemente I.C., Escera C. The role of the dopamine transporter DAT1 genotype on the neural correlates of cognitive flexibility. European Journal of Neuroscience 2010, 31:754-760.
58. Cools R., Roberts A.C., Robbins T.W. Serotoninergic regulation of emotional and behavioural control processes. Trends in Cognitive Sciences 2008, 12:31-40.
59. Maier S.F., Watkins L.R. Role of the medial prefrontal cortex in coping and resilience. Brain Research 2010, 1355:52-60.
60. Bertolino A., Fazio L., Di G.A., Blasi G., Romano R., Taurisano P., et al. Genetically determined interaction between the dopamine transporter and the D2 receptor on prefronto-striatal activity and volume in humans. Journal of Neuroscience 2009, 29:1224-1234.
61. Cohen J.D., Castro-Alamancos M.A. Early sensory pathways for detection of fearful conditioned stimuli: tectal and thalamic relays. Journal of Neuroscience 2007, 27:7762-7776.
62. Morris J.S., Buchel C., Dolan R.J. Parallel neural responses in amygdala subregions and sensory cortex during implicit fear conditioning. Neuroimage 2001, 13:1044-1052.
63. Crane L., Goddard L., Pring L. Sensory processing in adults with autism spectrum disorders. Autism 2009, 13:215-228.
64. Reynolds S., Lane S.J. Sensory overresponsivity and anxiety in children with ADHD. American Journal of Occupational Therapy 2009, 63:433-440.
65. Bryant R.A., Felmingham K.L., Kemp A.H., Barton M., Peduto A.S., Rennie C., et al. Neural networks of information processing in posttraumatic stress disorder: a functional magnetic resonance imaging study. Biological Psychiatry 2005, 58:111-118.
66. Aubert-Khalfa S., Granier J.P., Reynaud E., El K.M., Grosse E.M., Samuelian J.C., et al. Pure-tone auditory thresholds are decreased in depressed people with post-traumatic stress disorder. Journal of Affective Disorders 2010, 127:169-176.
67. Hegerl U., Himmerich H., Engmann B., Hensch T. Mania and attention-deficit/hyperactivity disorder: common symptomatology, common pathophysiology and common treatment?. Current Opinion in Psychiatry 2010, 23:1-7.
68. Alsene K.M., Bakshi V.P. Pharmacological stimulation of locus coeruleus reveals a new antipsychotic-responsive pathway for deficient sensorimotor gating. Neuropsychopharmacology 2011, 36:1656-1667.
69. Pinault D. Dysfunctional thalamus-related networks in schizophrenia. Schizophrenia Bulletin 2011, 37:238-243.
70. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 2010, 36:529-538.
71. Davis M., Walker D.L., Miles L., Grillon C. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010, 35:105-135.
72. Fanselow M.S. From contextual fear to a dynamic view of memory systems. Trends in Cognitive Sciences 2010, 14:7-15.
73. Phillips R.G., LeDoux J.E. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learning and Memory 1994, 1:34-44.
74. Selden N.R., Robbins T.W., Everitt B.J. Enhanced behavioral conditioning to context and impaired behavioral and neuroendocrine responses to conditioned stimuli following ceruleocortical noradrenergic lesions: support for an attentional hypothesis of central noradrenergic function. Journal of Neuroscience 1990, 10:531-539.
75. Soliman F., Glatt C.E., Bath K.G., Levita L., Jones R.M., Pattwell S.S., et al. A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 2010, 327:863-866.
76. Bach D.R., Grandjean D., Sander D., Herdener M., Strik W.K., Seifritz E. The effect of appraisal level on processing of emotional prosody in meaningless speech. Neuroimage 2008, 42:919-927.
77. 2+ channels in ACC. Nature Neuroscience 2010, 13:482-488.
78. Killcross S., Robbins T.W., Everitt B.J. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 1997, 388:377-380.
79. Etkin A., Egner T., Peraza D.M., Kandel E.R., Hirsch J. Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 2006, 51:871-882.
80. Britton J.C., Gold A.L., Deckersbach T., Rauch S.L. Functional MRI study of specific animal phobia using an event-related emotional counting stroop paradigm. Depression and Anxiety 2009, 26:796-805.
81. Steinberg L., Tremblay A.M., Zack M., Busto U.E., Zawertailo L.A. Effects of stress and alcohol cues in men with and without problem gambling and alcohol use disorder. Drug and Alcohol Dependence 2011, 119:46-55.
82. Besnier N., Kaladjian A., Mazzola-Pomietto P., Adida M., Fakra E., Jeanningros R., et al. Differential responses to emotional interference in paranoid schizophrenia and bipolar mania. Psychopathology 2011, 44:1-11.
83. Rao N.P., Arasappa R., Reddy N.N., Venkatasubramanian G., Reddy Y.C. Emotional interference in obsessive-compulsive disorder: a neuropsychological study using optimized emotional Stroop test. Psychiatry Research 2010, 180:99-104.
84. Fineberg N.A., Potenza M.N., Chamberlain S.R., Berlin H.A., Menzies L., Bechara A., et al. Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology 2010, 35:591-604.
85. Patrick C.J., Fowles D.C., Krueger R.F. Triarchic conceptualization of psychopathy: developmental origins of disinhibition, boldness, and meanness. Development and Psychopathology 2009, 21:913-938.
86. Boyd B.A., McBee M., Holtzclaw T., Baranek G.T., Bodfish J.W. Relationships among repetitive behaviors, sensory features, and executive functions in high functioning autism. Research in Autism Spectrum Disorders 2009, 3:959-966.
87. Sesack S.R., Grace A.A. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 2010, 35:27-47.
88. Solanto M.V., Abikoff H., Sonuga-Barke E., Schachar R., Logan G.D., Wigal T., et al. The ecological validity of delay aversion and response inhibition as measures of impulsivity in AD/HD: a supplement to the NIMH multimodal treatment study of AD/HD. Journal of Abnormal Child Psychology 2001, 29:215-228.
89. Cardinal R.N., Robbins T.W., Everitt B.J. The effects of d-amphetamine, chlordiazepoxide, alpha-flupenthixol and behavioural manipulations on choice of signalled and unsignalled delayed reinforcement in rats. Psychopharmacology 2000, 152:362-375.
90. Cardinal R.N., Pennicott D.R., Sugathapala C.L., Robbins T.W., Everitt B.J. Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 2001, 292:2499-2501.
91. Winstanley C.A., Theobald D.E., Cardinal R.N., Robbins T.W. Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. Journal of Neuroscience 2004, 24:4718-4722.
92. McClure S.M., Laibson D.I., Loewenstein G., Cohen J.D. Separate neural systems value immediate and delayed monetary rewards. Science 2004, 306:503-507.
93. Eagle D.M., Robbins T.W. Inhibitory control in rats performing a stop-signal reaction-time task: effects of lesions of the medial striatum and d-amphetamine. Behavioral Neuroscience 2003, 117:1302-1317.
94. Menzies L., Williams G.B., Chamberlain S.R., Ooi C., Fineberg N., Suckling J., et al. White matter abnormalities in patients with obsessive-compulsive disorder and their first-degree relatives. American Journal of Psychiatry 2008, 165:1308-1315.
95. Elliott R., Sahakian B.J., McKay A.P., Herrod J.J., Robbins T.W., Paykel E.S. Neuropsychological impairments in unipolar depression: the influence of perceived failure on subsequent performance. Psychological Medicine 1996, 26:975-989.
96. Murphy F.C., Michael A., Robbins T.W., Sahakian B.J. Neuropsychological impairment in patients with major depressive disorder: the effects of feedback on task performance. Psychological Medicine 2003, 33:455-467.
97. Corbett B.A., Constantine L.J., Hendren R., Rocke D., Ozonoff S. Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development. Psychiatry Research 2009, 166:210-222.
98. Clarke H.F., Robbins T.W., Roberts A.C. Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. Journal of Neuroscience 2008, 28:10972-10982.
99. Dias R., Robbins T.W., Roberts A.C. Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behavioral Neuroscience 1996, 110:872-886.
100. McAlonan K., Brown V.J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behavioural Brain Research 2003, 146:97-103.
101. Birrell J.M., Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. Journal of Neuroscience 2000, 20:4320-4324.
102. Ragozzino M.E. The effects of dopamine D(1) receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. Learning and Memory 2002, 9:18-28.
103. Floresco S.B., Block A.E., Tse M.T. Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behavioural Brain Research 2008, 190:85-96.
104. Bissonette G.B., Martins G.J., Franz T.M., Harper E.S., Schoenbaum G., Powell E.M. Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. Journal of Neuroscience 2008, 28:11124-11130.
105. Dias R., Robbins T.W., Roberts A.C. Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin Card Sort Test: restriction to novel situations and independence from on-line processing. Journal of Neuroscience 1997, 17:9285-9297.
106. Bussey T.J., Holmes A., Lyon L., Mar A.C., McAllister K.A., Nithianantharajah J., et al. New translational assays for preclinical modelling of cognition in schizophrenia: the touchscreen testing method for mice and rats. Neuropharmacology 2011, 62:1191-1203.
107. Purgert R.J., Wheeler D.S., McDannald M.A., Holland P.C. Role of amygdala central nucleus in aversive learning produced by shock or by unexpected omission of food. Journal of Neuroscience 2012, 32:2461-2472.
108. Homberg J.R., Pattij T., Janssen M.C., Ronken E., De Boer S.F., Schoffelmeer A.N., et al. Serotonin transporter deficiency in rats improves inhibitory control but not behavioural flexibility. European Journal of Neuroscience 2007, 26:2066-2073.
109. Enkel T., Gholizadeh D., von Bohlen Und H.O., Sanchis-Segura C., Hurlemann R., Spanagel R., et al. Ambiguous-cue interpretation is biased under stress- and depression-like states in rats. Neuropsychopharmacology 2010, 35:1008-1015.
110. Etkin A., Klemenhagen K.C., Dudman J.T., Rogan M.T., Hen R., Kandel E.R., et al. Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 2004, 44:1043-1055.
111. Fusar-Poli P., Placentino A., Carletti F., Landi P., Allen P., Surguladze S., et al. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience 2009, 34:418-432.
112. Whalen P.J., Rauch S.L., Etcoff N.L., McInerney S.C., Lee M.B., Jenike M.A. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience 1998, 18:411-418.
113. Harrison A.A., Everitt B.J., Robbins T.W. Central serotonin depletion impairs both the acquisition and performance of a symmetrically reinforced go/no-go conditional visual discrimination. Behavioural Brain Research 1999, 100:99-112.
114. Crockett M.J., Clark L., Robbins T.W. Reconciling the role of serotonin in behavioral inhibition and aversion: acute tryptophan depletion abolishes punishment-induced inhibition in humans. Journal of Neuroscience 2009, 29:11993-11999.
115. Cools R., Clark L., Owen A.M., Robbins T.W. Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. Journal of Neuroscience 2002, 22:563-567.
116. Bari A., Theobald D.E., Caprioli D., Mar A.C., Aidoo-Micah A., Dalley J.W., et al. Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacology 2010, 35:1290-1301.
117. Chamberlain S.R., Sahakian B.J. The neuropsychiatry of impulsivity. Current Opinion in Psychiatry 2007, 20:255-261.
118. 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.
119. Chamberlain S.R., Fineberg N.A., Blackwell A.D., Robbins T.W., Sahakian B.J. Motor inhibition and cognitive flexibility in obsessive-compulsive disorder and trichotillomania. American Journal of Psychiatry 2006, 163:1282-1284.
120. Hollander E., Wong C.M. Obsessive-compulsive spectrum disorders. Journal of Clinical Psychiatry 1995, 56(Suppl. 4):3-6.
121. Joel D., Avisar A. Excessive lever pressing following post-training signal attenuation in rats: a possible animal model of obsessive compulsive disorder?. Behavioural Brain Research 2001, 123:77-87.
122. Szechtman H., Sulis W., Eilam D. Quinpirole induces compulsive checking behavior in rats: a potential animal model of obsessive-compulsive disorder (OCD). Behavioral Neuroscience 1998, 112:1475-1485.
123. Tsaltas E., Kontis D., Chrysikakou S., Giannou H., Biba A., Pallidi S., et al. Reinforced spatial alternation as an animal model of obsessive-compulsive disorder (OCD): investigation of 5-HT2C and 5-HT1D receptor involvement in OCD pathophysiology. Biological Psychiatry 2005, 57:1176-1185.
124. Clarke H.F., Walker S.C., Dalley J.W., Robbins T.W., Roberts A.C. Cognitive inflexibility after prefrontal serotonin depletion is behaviorally and neurochemically specific. Cerebral Cortex 2007, 17:18-27.
125. Endrass T., Kloft L., Kaufmann C., Kathmann N. Approach and avoidance learning in obsessive-compulsive disorder. Depression and Anxiety 2011, 28:166-172.
126. Carola V., Frazzetto G., Pascucci T., Audero E., Puglisi-Allegra S., Cabib S., et al. Identifying molecular substrates in a mouse model of the serotonin transporter×environment risk factor for anxiety and depression. Biological Psychiatry 2008, 63:840-846.
127. van den Hove D.L., Jakob S.B., Schraut K.G., Kenis G., Schmitt A.G., Kneitz S., et al. Differential effects of prenatal stress in 5-Htt deficient mice: towards molecular mechanisms of gene×environment interactions. PLoS One 2011, 6:e22715.
128. Homberg JR, van den Hove DL. The serotonin transporter gene and functional and pathological adaptation to environmental variation across the life span. Progress in Neurobiology, in press. doi:10.1016/j.pneurobio.2012.08.003.
129. Singewald N. Altered brain activity processing in high-anxiety rodents revealed by challenge paradigms and functional mapping. Neuroscience and Biobehavioral Reviews 2007, 31:18-40.
130. Dalley J.W., Fryer T.D., Aigbirhio F.I., Brichard L., Richards H.K., Hong Y.T., et al. Modelling human drug abuse and addiction with dedicated small animal positron emission tomography. Neuropharmacology 2009, 56(Suppl. 1):9-17.
131. Bruns A., Künnecke B., Risterucci C., Moreau J.L., von Kienlin M. Validation of cerebral blood perfusion imaging as a modality for quantitative pharmacological MRI in rats. Magnetic Resonance in Medicine 2009, 61:1451-1458.
132. Hefner K., Whittle N., Juhasz J., Norcross M., Karlsson R.M., Saksida L.M., et al. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. Journal of Neuroscience 2008, 28(14):8074-8085.
133. Harro J., Kanarik M., Matrov D., Panksepp J. Mapping patterns of depression-related brain regions with cytochrome oxidase histochemistry: relevance of animal affective systems to human disorders, with a focus on resilience to adverse events. Neuroscience and Biobehavioral Reviews 2011, 35:1876-1889.
134. Belin D., Everitt B.J. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 2008, 57:432-441.
135. Parkinson J.A., Willoughby P.J., Robbins T.W., Everitt B.J. Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. Behavioral Neuroscience 2000, 114:42-63.
136. Gunduz-Cinar O., Macpherson K.P., Cinar R., Gamble-George J., Sugden K., Williams B., et al. Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity. Molecular Psychiatry 2012, 10.1038/mp.2012.72.
137. Zhang F., Gradinaru V., Adamantidis A.R., Durand R., Airan R.D., de L.L., et al. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nature Protocols 2010, 5:439-456.
138. Tye K.M., Prakash R., Kim S.Y., Fenno L.E., Grosenick L., Zarabi H., et al. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 2011, 471:358-362.