Frontal responses during learning predict vulnerability to the psychotogenic effects of ketamine: Linking cognition, brain activity, and psychosis

Archives of General Psychiatry

Volumn 63, Issue 6, 2006, Pages 611-621

  Corlett, Philip R ^a   Honey, Garry D ^a   Aitken, Michael R F ^b   Dickinson, Anthony ^b   Shanks, David R ^c   Absalom, Anthony R ^a   Lee, Michael ^a   Pomarol Clotet, Edith ^a   Murray, Graham K ^a   McKenna, Peter J ^a   Robbins, Trevor W ^b   Bullmore, Edward T ^a   Fletcher, Paul C ^a,d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UK   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; PSYCHEDELIC AGENT;

ADULT; ARTICLE; CONTROLLED STUDY; DELUSION; ELECTROENCEPHALOGRAM; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERCEPTION DISORDER; PSYCHOGENESIS; RIGHT HANDEDNESS; SCORING SYSTEM; STATE DEPENDENT LEARNING; STRUCTURED INTERVIEW; THEORETICAL MODEL;

ADULT; ASSOCIATION LEARNING; BRIEF PSYCHIATRIC RATING SCALE; COGNITION DISORDERS; DELUSIONS; DISEASE SUSCEPTIBILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FRONTAL LOBE; HUMANS; KETAMINE; MAGNETIC RESONANCE IMAGING; MALE; MODELS, THEORETICAL; PERCEPTUAL DISORDERS; PLACEBOS; PROBABILITY; PSYCHIATRIC STATUS RATING SCALES; PSYCHOSES, SUBSTANCE-INDUCED; PSYCHOTIC DISORDERS;

EID: 33744924921     PISSN: 0003990X     EISSN: 15383636     Source Type: Journal    
DOI: 10.1001/archpsyc.63.6.611     Document Type: Article

References (74)

1. Miller R. Schizophrenic psychology, associative learning and forebrain dopamine. Med Hypotheses. 1976;2:203-211.
2. Miller R. Hyperactivity of associations in psychosis. Aust N Z J Psychiatry. 1989;23:241-248.
3. Miller R. Striatal dopamine in reward and attention: a system for understanding the symptomatology of acute schizophrenia and mania. Int Rev Neurobiol. 1993;35:161-278.
4. Gray JA, Feldon J, Rawlins JNP, Hemsley DR, Smith AD. The neuropsychology of schizophrenia. Behav Brain Sci. 1991;14:1-20.
5. Hemsley DR. Perceptual and cognitive abnormalities as the bases for schizophrenic symptoms. In: David A, Cutting J, eds. The Neuropsychology of Schizophrenia. Hove, United Kingdom: Psychology Press; 1994:97-116.
6. Kapur S. Psychosis as a state of aberrant salience: a framework linking biology, phenomenology and pharmacology in schizophrenia. Am J Psychiatry. 2003;160:13-23.
7. Kapur S. How antipsychotics become anti-"psychotic": from dopamine to salience to psychosis. Trends Pharmacol Sci. 2004;25:402-406.
8. Kapur S, Mizrahi R, Li M. From dopamine to salience to psychosis: linking biology, pharmacology and phenomenology of psychosis. Schizophr Res. 2005;79:59-68.
9. Matussek P. Untersuchungen uber die wahnwahrnehmung. Psychiatri Z Neurol. 1952;189:279-318.
10. McGhie A, Chapman J. Disorders of attention and perception in early schizophrenia. Br J Med Psychol. 1961;34:103-116.
11. Bowers MB Jr, Freedman DX. "Psychedelic" experiences in acute psychoses. Arch Gen Psychiatry. 1966;15:240-248.
12. Chapman J. The early symptoms of schizophrenia. Br J Psychiatry. 1966;112:225-251.
13. Bowers MB Jr. Pathogenesis of acute schizophrenia: an experimental approach. Arch Gen Psychiatry. 1968;19:348-355.
14. Freedman B, Chapman LJ. Early subjective experience of schizophrenic episodes. J Abnorm Psychol. 1973;82:46-54.
15. Freedman BJ. The subjective experience of perceptual and cognitive abnormalities in schizophrenia: a review of autobiographical accounts. Arch Gen Psychiatry. 1974;30:333-340.
16. Schneider C. Die Psychologie der Schizophrenen. Leipzig, Germany: Germany Thieme; 1930.
17. Rescorla RA, Wagner AR. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and non-reinforcement. In: Black AH, Prokasy WF, eds. Classical Conditioning II: Current Research and Theory. New York, NY: Appleton-Century-Crofts; 1972:64-99.
18. Mackintosh NJ. A theory of attention: variations in the associability of stimuli with reinforcement. Psychol Rev. 1975;82:276-298.
19. Pearce JM, Hall G. A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol Rev. 1980;87:532-552.
20. Dickinson A. The 28th Bartlett Memorial Lecture: causal learning: an associative analysis. Q J Exp Psychol B. 2001;54:3-25.
21. Schultz W. The phasic reward signal of primate dopamine neurons. Adv Pharmacol. 1998;42:686-690.
22. Hollerman JR, Schultz W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat Neurosci. 1998;1:304-309.
23. Schultz W, Dickinson A. Neural coding of prediction errors. Annu Rev Neurosci. 2000;23:473-500.
24. Waelti P, Dickinson A, Schultz W. Dopamine responses comply with basic assumptions of formal learning theory. Nature. 2001;412:43-48.
25. Fletcher PC, Anderson JM, Shanks DR, Honey R, Carpenter TA, Papadakis N, Bullmore ET. Responses of human frontal cortex to surprising events are predicted by formal associative learning theory. Nat Neurosci. 2001;4:1043-1048.
26. O'Doherty JP, Dayan P, Friston K, Critchley H, Dolan RJ. Temporal difference models and reward-related learning in the human brain. Neuron. 2003;38:329-337.
27. McClure SM, Berns G S, Montague PR. Temporal prediction errors in a passive learning task activate human striatum. Neuron. 2003;38:339-346.
28. Turner DC, Aitken MR, Shanks DR, Sahakian BJ, Robbins TW, Schwarzbauer C, Fletcher PC. The role of lateral frontal cortex in causal associative learning: exploring preventative and super-learning. Cereb Cortex. 2004;14:872-880.
29. Corlett PR, Aitken MR, Dickinson A, Shanks DR, Honey GD, Honey RA, Robbins TW, Bullmore ET, Fletcher PC. Prediction error during retrospective revaluation of causal associations in humans: fMRI evidence in favor of an associative model of learning. Neuron. 2004;44:877-888.
30. Ghoneim MM, Hinrichs JV, Mewaldt SP, Petersen RC. Ketamine: behavioral effects of subanesthetic doses. J Clin Psychopharmacol. 1985;5:70-77.
31. Krystal JH, Karper LP, Seibyl JP, Freeman JK, Delaney R, Bremner JD, Heninger GR, Bowers MB Jr, Charney DS. Subanesthetic effects of the non-competitive NMDA antagonist, ketamine, in humans: psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry. 1994;51:199-214.
32. Bowdle TA, Radant AD, Cowley DS, Karasch ED, Roy-Byrne PP. Psychedelic effects of ketamine in healthy volunteers: relationship to steady-state plasma concentrations. Anesthesiology. 1998;88:82-88.
33. Krystal JH, Bennet A, Abi-Saab D, Belger A, Karper LP, D'Souza DC, Lipschitz D, Abi-Dargham A, Charney DS. Dissociation of ketamine effects on rule acquisition and rule implementation: possible relevance to NMDA receptor contributions to executive cognitive functions. Biol Psychiatry. 2000;47:137-143.
34. Malhotra AK, Pinals DA, Weingartner H, Sirocco K, Missar CD, Pickar D, Breier A. NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Neuropsychopharmacology. 1996;14:301-307.
35. Adler CM, Goldberg TE, Malhotra AK, Pickar D, Brier A. Effects of ketamine on thought disorder, working memory, and semantic memory in healthy volunteers. Biol Psychiatry. 1998;43:811-816.
36. Newcomer JW, Farber NB, Jetovic-Terodovic V, Selke G, Melson AK, Hershey T, Craft S, Olney JW. Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis. Neuropsychopharmacology. 1999;20:106-118.
37. Umbricht D, Schmidt L, Koller R, Vollenweider FX, Hell D, Javitt DC. Ketamine-induced deficits in auditory and visual context-dependent processing in healthy volunteers: implications for models of cognitive deficits in schizophrenia. Arch Gen Psychiatry. 2000;57:1139-1147.
38. Umbricht D, Koller R, Vollenweider FX, Schmid L. Mismatch negativity predicts psychotic experiences induced by NMDA receptor antagonist in healthy volunteers. Biol Psychiatry. 2002;51:400-406.
39. Duncan EJ, Madonick SH, Parwani A, Angrist B, Rajan R, Chakravorty S, Efferen TR, Sziliagy S, Stephanides M, Chappell PB, Gonzenbach S, Ko GN, Rotrosen JP. Clinical and sensorimotor gating effects of ketamine in normals. Neuropsychopharmacology. 2001;25:72-83.
40. Lahti AC, Weiler MA, Tamara-Michaelidis BA, Parwani A, Tamminga CA. Effects of ketamine in normal and schizophrenic volunteers. Neuropsychopharmacology. 2001;25:455-467.
41. Abel KM, Allin MP, Hemsley DR, Geyer MA. Low dose ketamine increases prepulse inhibition in healthy men. Neuropharmacology. 2003;44:729-737.
42. Honey RA, Turner DC, Honey GD, Sharar SR, Kumaran D, Pomarol-Clotet E, McKenna P, Sahakian BJ, Robbins TW, Fletcher PC. Subdissociative dose ketamine produces a deficit in manipulation but not maintenance of the contents of working memory. Neuropsychopharmacology. 2003;28:2037-2044.
43. Morgan CJ, Mofeez A, Bradner B, Bromley L, Curran HV. Acute effects of ketamine on memory systems and psychotic symptoms in healthy volunteers. Neuropsychopharmacology. 2004;29:208-218.
44. Morgan CJ, Mofeez A, Bradner B, Bromley L, Curran HV. Ketamine impairs response inhibition and is positively reinforcing in healthy volunteers: a dose-response study. Psychopharmacology (Berl). 2004;172:298-308.
45. Honey GD, Honey RA, Sharar SR, Turner DC, Pomarol-Clotet E, Kumaran D, Simons JS, Hu X, Rugg MD, Bullmore ET, Fletcher PC. Impairment of specific episodic memory processes by sub-psychotic doses of ketamine: the effects of levels of processing at encoding and of the subsequent retrieval task [published online ahead of print October 12, 2005]. Psychopharmacology. 2005;181:445-457. doi:10.1007/s00213-005-0001-z. Accessed October 12, 2005.
46. Honey GD, O'Loughlin C, Turner DC, Pomarol-Clotet E, Corlett PR, Fletcher PC. The effects of a subpsychotic dose of ketamine on recognition and source memory for agency: implications for pharmacological modelling of core symptoms of schizophrenia [published online ahead of print August 3, 2005]. Neuropsychopharmacology. 2006;31:413-423. doi:10.1038/sj.npp.1300846. Accessed August 3, 2005.
47. Vollenweider FX, Leenders KL, Scharfetter C, Antonini A, Maguire P, Missimer J, Angst J. Metabolic hyperfrontality and psychopathology in the ketamine model of psychosis using positron emission tomography (PET) and [18F]fluorodeoxyglucose (FDG). Eur Neuropsychopharmacol. 1997;7:9-24.
48. Vollenweider FX, Leenders KL, Oye I, Hell D, Angst J. Differential psychopathology and patterns of cerebral glucose utilisation produced by (S)- and (R)-ketamine in healthy volunteers using positron emission tomography (PET). Eur Neuropsychopharmacol. 1997;7:25-38.
49. Breier A, Malhotra AK, Pinals DA, Weisenfeld NI, Pickar D. Association of ketamineinduced psychosis with focal activation of the prefrontal cortex in healthy volunteers. Am J Psychiatry. 1997;154:805-811.
50. Breier A, Adler CM, Weisenfeld N, Su TP, Elman I, Picken L, Malhotra AK, Pickar D. Effects of NMDA antagonism on striatal dopamine release in healthy subjects: application of a novel PET approach. Synapse. 1998;29:142-147.
51. Holcomb HH, Lahti AC, Medoff DR, Weiler M, Tamminga CA. Sequential regional cerebral blood flow brain scans using PET with H2(15)O demonstrate ketamine actions in CNS dynamically. Neuropsychopharmacology. 2001;25:165-172.
52. Kegeles LS, Martinez D, Kochan LD, Hwang DR, Huang Y, Malawi O, Suckow RF, Van Heertum RL, Laruelle M. NMDA antagonist effects on striatal dopamine release: positron emission tomography studies in humans. Synapse. 2002;43:19-29.
53. Abel KM, Allin MP, Kucharska-Pietura K, David AS, Andrew C, Williams S, Brammer MJ, Phillips ML. Ketamine alters neural processing of facial emotion recognition in healthy men: an fMRI study. Neuroreport. 2003;14:387-391.
54. Abel KM, Allin MP, Kucharska-Pietura K, Andrew C, Williams S, David AS, Phillips ML. Ketamine and fMRI BOLD signal: distinguishing between effects mediated by change in blood flow versus change in cognitive state. Hum Brain Mapp. 2003;18:135-145.
55. Honey RA, Honey GD, O'Loughlin C, Sharar SR, Kumaran D, Bullmore ET, Menon DK, Donovan T, Lupson VC, Bisbrowne-Chippendale R, Fletcher PC. Acute ketamine administration alters the brain responses to executive demands in a verbal working memory task: an FMRI study. Neuropsychopharmacology. 2004;29:1203-1214.
56. Northoff G, Richter A, Bermpohl F, Grimm S, Martin E, Marcar VL, Wahl C, Hell D, Boeker H. NMDA hypofunction in the posterior cingulate as a model for schizophrenia: an exploratory ketamine administration study in fMRI. Schizophr Res. 2005;72:235-248.
57. Honey GD, Honey RA, O'Loughlin C, Sharar SR, Suckling J, Menon DK, Sleator C, Bullmore ET, Fletcher PC. Ketamine disrupts frontal and hippocampal contribution to encoding and retrieval of episodic memory: an fMRI study. Cereb Cortex. 2005;15:749-759.
58. Nelson H. National Adult Reading Test Manual. Windsor, United Kingdom: nfer Nelson; 1982.
59. Domino EF, Zsigmond EK, Domino LE, Domino KE, Kothary SP, Domino SE. Plasma levels of ketamine and two of its metabolites in surgical patients using a gas chromatographic mass fragmentographic assay. Anesth Analg. 1982;61:87-92.
60. Wing J, Cooper J, Sartorius N. Measurement and Classification of Psychiatric Symptoms: An Instruction Manual for the PSE and CATEGO Program. New York, NY: Cambridge University Press; 1974.
61. Bremner JD, Krystal JH, Putnam FW, Southwick SM, Marmar C, Charney DS, Mazure CM. Measurement of dissociative states with the Clinician-Administered Dissociative States Scale (CADSS). J Trauma Stress. 1998;11:125-136.
62. Ventura J, Lukoff D, Nuechterlein KH, Lieberman RP, Green M, Shaner A. Appendix 1: brief Psychiatric Ratings Scale (BPRS) Expanded Version (4.0) scales, anchor points and administration manual. Int J Methods Psychiatr Res. 1993;3:227-243.
63. Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, Turner R. Event-related fMRI: characterizing differential responses. Neuroimage. 1998;7:30-40.
64. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage. 2002;15:870-878.
65. Knutson B, Bjork JM, Fong GW, Hommer D, Mattay VS, Weinberger DR. Amphetamine modulates human incentive processing. Neuron. 2004;43:261-269.
66. Dreher JC, Kohn P, Berman KF. Neural coding of distinct statistical properties of reward information in humans [published online ahead of print July 20, 2005]. Cereb Cortex. 2006;16:561-573. http://cercor.oxfordjournals.org/cgi/ content/full/16/4/561. Accessed July 20, 2005.
67. Zink CF, Pagnoni G, Martin ME, Dhamala M, Berns GS. Human striatal response to salient nonrewarding stimuli. J Neurosci. 2003;23:8092-8097.
68. Aron AR, Shohamy D, Clark J, Myers C, Gluck MA, Poldrack RA. Human midbrain sensitivity to cognitive feedback and uncertainty during classification learning. J Neurophysiol. 2004;92:1144-1152.
69. Rodriguez PF, Aron AR, Poldrack RA. Ventral-striatal/nucleus-accumbens sensitivity to prediction errors during classification learning [published online ahead of print August 9, 2005]. Hum Brain Mapp. 2006;27:306-313. doi:10.1002/hbm.20186. Accessed August 9, 2005.
70. Huettel SA, Song AW, McCarthy G. Decisions under uncertainty: probabilistic context influences activity of prefrontal and parietal cortices. J Neurosci. 2005;25:3304-3311.
71. Callicott JH, Bertolino A, Mattay VS, Langheim FJ, Duyn J, Coppola R, Goldberg TE, Weinberger DR. Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cereb Cortex. 2000;10:1078-1082.
72. Umbricht D, Krljes S. Mismatch negativity in schizophrenia: a meta-analysis. Schizophr Res. 2005;76:1-23.
73. Lavin A, Nogueira L, Lapish CC, Wightman RM, Phillips PE, Seamans JK. Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signalling. J Neurosci. 2005;25:5013-5023.
74. Fletcher PC. Functional neuroimaging of psychiatric disorders: exploring hidden behaviour. Psychol Med. 2004;34:577-581.