Amphetamine sensitisation and memory in healthy human volunteers: A functional magnetic resonance imaging study

Journal of Psychopharmacology

Volumn 28, Issue 9, 2014, Pages 857-865

  O'Daly, Owen G ^a   Joyce, Daniel ^a   Tracy, Derek K ^a,b   Stephan, Klaas E ^c,d   Murray, Robin M ^a   Shergill, Sukhwinder ^a,e  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b OXLEAS NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e SOUTH LONDON AND MAUDSLEY NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Amphetamine; dopamine; medial temporal lobe; midbrain; motor learning; sensitisation

Indexed keywords

DEXAMPHETAMINE; PLACEBO; CENTRAL STIMULANT AGENT;

ARTICLE; ATTENTION; BOLD SIGNAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG EXPOSURE; ENTORHINAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; HYPERACTIVITY; LEARNING; MEMORY CONSOLIDATION; MESENCEPHALON; NORMAL HUMAN; PARALLEL DESIGN; PRIORITY JOURNAL; SCHIZOPHRENIA; SENSITIZATION; SUBICULUM; SUBSTANTIA NIGRA; TASK PERFORMANCE; TEMPORAL LOBE; VENTRAL TEGMENTUM; VOLUNTEER; CENTRAL NERVOUS SYSTEM SENSITIZATION; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; FUNCTIONAL NEUROIMAGING; MEMORY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL;

ATTENTION; CENTRAL NERVOUS SYSTEM SENSITIZATION; CENTRAL NERVOUS SYSTEM STIMULANTS; DEXTROAMPHETAMINE; DOUBLE-BLIND METHOD; FUNCTIONAL NEUROIMAGING; HEALTHY VOLUNTEERS; HUMANS; MAGNETIC RESONANCE IMAGING; MEMORY; MESENCEPHALON; SERIAL LEARNING; TEMPORAL LOBE;

EID: 84906043870     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881114527360     Document Type: Article

References (63)

1. Adams RA, Stephan KE, Brown HR, et al. The computational anatomy of psychosis. Front Psychiatry. 2013 ; 4: 47
2. Adcock RA, Thangavel A, Whitfield-Gabrieli S, et al. Reward-motivated learning: Mesolimbic activation precedes memory formation. Neuron. 2006 ; 50: 507-517
3. Adler LE, Waldo MC. Counterpoint: A sensory gating-hippocampal model of schizophrenia. Schizophr Bull. 1991 ; 17: 19-24
4. Amunts K, Kedo O, Kindler M, et al. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps. Anat Embryol (Berl). 2005 ; 210: 343-352
5. Bertolino A, Saunders RC, Mattay VS, et al. Altered development of prefrontal neurons in rhesus monkeys with neonatal mesial temporo-limbic lesions: A proton magnetic resonance spectroscopic imaging study. Cereb Cortex. 1997 ; 7: 740-748
6. Boileau I, Dagher A, Leyton M, et al. Modelling sensitisation to stimulants in humans: An [11C]raclopride/positron emission tomography study in healthy men. Arch Gen Psychiatry. 2006 ; 63: 1386-1395
7. Bunsey M, Eichenbaum H. Critical role of the parahippocampal region for paired-associate learning in rats. Behav Neurosci. 1993 ; 107: 740-747
8. Dolan RJ, Fletcher PC. Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature. 1997 ; 388: 582-585
9. Dusek JA, Eichenbaum H. The hippocampus and memory for orderly stimulus relations. Proc Natl Acad Sci U S A. 1997 ; 94: 7109-7114
10. Eickhoff SB, Stephan KE, Mohlberg H, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005 ; 25: 1325-1335
11. Ergorul C, Eichenbaum H. Essential role of the hippocampal formation in rapid learning of higher-order sequential associations. J Neurosci. 2006 ; 26: 4111-4117
12. Eyler LT, Jeste DV, Brown GG. Brain response abnormalities during verbal learning among patients with schizophrenia. Psychiatry Res. 2008 ; 162: 11-25
13. Friston KJ, Fletcher P, Josephs O, et al. Event-related fMRI: Characterising differential responses. Neuroimage. 1998 ; 7: 30-40
14. Fletcher PC, Frith CD. Perceiving is believing: A Bayesian approach to explaining the positive symptoms of schizophrenia. Nat Rev Neurosci. 2009 ; 10: 48-58
15. Friston KJ, Grasby PM, Bench CJ, et al. Measuring the neuromodulatory effects of drugs in man with positron emission tomography. Neurosci Lett. 1992 ; 141: 106-110
16. Friston KJ, Holmes AP, Poline JB, et al. Analysis of fMRI time-series revisited. Neuroimage. 1995 ; 2: 45-53
17. George D, Hawkins J. Towards a mathematical theory of cortical micro-circuits. PLoS Comput Biol. 2009 ; 5: e1000532
18. Gheysen F, Van Opstal F, Roggeman C, et al. Hippocampal contribution to early and later stages of implicit motor sequence learning. Exp Brain Res. 2010 ; 202: 795-807
19. Gray JA, Joseph MH, Hemsley DR, et al. The role of mesolimbic dopaminergic and retrohippocampal afferents to the nucleus accumbens in latent inhibition: Implications for schizophrenia. Behav Brain Res. 1995 ; 71: 19-31
20. Haertzen CA, Hickey JE Methods of assessing the reinforcing properties of abused drugs. Bozarth MA, ed. New York: Springer-Verlag ; 1987: 489-524.
21. Hikosaka O, Miyashita K, Miyachi S, et al. Differential roles of the frontal cortex, basal ganglia, and cerebellum in visuomotor sequence learning. Neurobiol Learn Mem. 1998 ; 70: 137-149
22. Howes OD, Kapur S. The dopamine hypothesis of schizophrenia: Version III-The final common pathway. Schizophr Bull. 2009 ; 35: 549-562
23. Hutton C, Bork A, Josephs O, et al. Image distortion correction in fMRI: A quantitative evaluation. Neuroimage. 2002 ; 16: 217-240
24. Kalivas PW, Duffy P. Time course of extracellular dopamine and behavioural sensitisation to cocaine. I. Dopamine axon terminals. J Neurosci. 1993 ; 13: 266-275
25. Kalivas PW, Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitisation of motor activity. Brain Res Brain Res Rev. 1991 ; 16: 223-244
26. 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
27. Kriegeskorte N, Simmons WK, Bellgowan PS, et al. Circular analysis in systems neuroscience: The dangers of double dipping. Nat Neurosci. 2009 ; 12: 535-540
28. Krishnan RR, Keefe R, Kraus M. Schizophrenia is a disorder of higher order hierarchical processing. Med Hypotheses. 2009 ; 72: 740-744
29. Laruelle M, Abi-Dargham A, Gil R, et al. Increased dopamine transmission in schizophrenia: Relationship to illness phases. Biol Psychiatry. 1999 ; 46: 56-72
30. Laruelle M, Abi-Dargham A, van Dyck CH, et al. Single photon emission computerised tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proc Natl Acad Sci U S A. 1996 ; 93: 9235-9240
31. Lipska BK, Jaskiw GE, Weinberger DR. Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: A potential animal model of schizophrenia. Neuropsychopharmacology. 1993 ; 9: 67-75
32. Lisman JE, Grace AA. The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron. 2005 ; 46: 703-713
33. Lodge DJ, Grace AA. Amphetamine activation of hippocampal drive of mesolimbic dopamine neurons: A mechanism of behavioural sensitisation. J Neurosci. 2008 ; 28: 7876-7882
34. McNair DM, Lorr M, Droppleman LF EdITS manual for the Profile of Mood States. San Diego: Educational and Industrial Testing Service ; 1992 :
35. Marvel CL, Schwartz BL, Howard DV, et al. Implicit learning of non-spatial sequences in schizophrenia. J Int Neuropsychol Soc. 2005 ; 11: 659-667
36. Mawlawi O, Martinez D, Slifstein M, et al. Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D(2) receptor parameter measurements in ventral striatum. J Cereb Blood Flow Metab. 2001 ; 21: 1034-1057
37. Meck WH, Penney TB, Pouthas V. Cortico-striatal representation of time in animals and humans. Curr Opin Neurobiol. 2008 ; 18: 145-152
38. O'Carroll CM, Martin SJ, Sandin J, et al. Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. Learn Mem. 2006 ; 13: 760-769
39. O'Daly OG, Guillin O, Tsapakis EM, et al. Schizophrenia and substance abuse co-morbidity: A role for dopamine sensitisation?. J Dual Diag. 2005 ; 1: 11-40
40. O'Daly OG, Joyce D, Stephan KE, et al. Functional magnetic resonance imaging investigation of the amphetamine sensitisation model of schizophrenia in healthy male volunteers. Arch Gen Psychiatry. 2011 ; 68: 545-554
41. Ongur D, Cullen TJ, Wolf DH, et al. The neural basis of relational memory deficits in schizophrenia. Arch Gen Psychiatry. 2006 ; 63: 356-365
42. Pedersen A, Siegmund A, Ohrmann P, et al. Reduced implicit and explicit sequence learning in first-episode schizophrenia. Neuropsychologia. 2008 ; 46: 186-195
43. Piazza PV, Deminiere JM, le Moal M, et al. Stress- and pharmacologically-induced behavioural sensitisation increases vulnerability to acquisition of amphetamine self-administration. Brain Res. 1990 ; 514: 22-26
44. Pilowsky LS, Kerwin RW, Murray RM. Schizophrenia: A neurodevelopmental perspective. Neuropsychopharmacology. 1993 ; 9: 83-91
45. Ragland JD, Gur RC, Valdez J, et al. Event-related fMRI of frontotemporal activity during word encoding and recognition in schizophrenia. Am J Psychiatry. 2004 ; 161: 1004-1015
46. Robinson TE, Becker JB. Enduring changes in brain and behaviour produced by chronic amphetamine administration: A review and evaluation of animal models of amphetamine psychosis. Brain Res. 1986 ; 396: 157-198
47. Roiser JP, Stephan KE, den Ouden HEM, et al. Do patients with schizophrenia exhibit aberrant salience?. Psychol Med. 2009 ; 39: 199-209
48. Sakai K, Hikosaka O, Miyauchi S, et al. Neural representation of a rhythm depends on its interval ratio. J Neurosci. 1999 ; 19: 10074-10081
49. Sax KW, Strakowski SM. Behavioural sensitisation in humans. J Addict Dis. 2001 ; 20: 55-65
50. Schendan HE, Searl MM, Melrose RJ, et al. An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron. 2003 ; 37: 1013-1025
51. Schendan HE, Searl MM, Melrose RJ, et al. Sequence? What Sequence?: the human medial temporal lobe and sequence learning. Mol Psychiatry. 2003 ; 8: 896-897
52. Schott BH, Sellner DB, Lauer CJ, et al. Activation of midbrain structures by associative novelty and the formation of explicit memory in humans. Learn Mem. 2004 ; 11: 383-387
53. Shenton ME, Dickey CC, Frumin M, et al. A review of MRI findings in schizophrenia. Schizophr Res. 2001 ; 49: 1-52
54. Shergill SS, Brammer MJ, Williams SC, et al. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch Gen Psychiatry. 2000 ; 57: 1033-1038
55. Stark CE, Squire LR. Simple and associative recognition memory in the hippocampal region. Learn Mem. 2001 ; 8: 190-197
56. Stephan KE, Baldeweg T, Friston KJ. Synaptic plasticity and dysconnection in schizophrenia. Biol Psychiatry. 2006 ; 59: 929-939
57. Stephan KE, Friston KJ, Frith CD. Dysconnection in schizophrenia: From abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull. 2009 ; 35: 509-527
58. Strakowski SM, Sax KW, Setters MJ, et al. Enhanced response to repeated d-amphetamine challenge: Evidence for behavioural sensitisation in humans. Biol Psychiatry. 1996 ; 40: 872-880
59. Strange BA, Duggins A, Penny W, et al. Information theory, novelty and hippocampal responses: Unpredicted or unpredictable?. Neural Netw. 2005 ; 18: 225-230
60. Todd CL, Grace AA. Modulation of ventral tegmental area dopamine cell activity by the ventral subiculum and entorhinal cortex. Ann N Y Acad Sci. 1999 ; 877: 688-690
61. Trumbo D, Noble M, Fowler F, et al. Motor performance on temporal tasks as a function of sequence length and coherence. J Exp Psychol. 1968 ; 77: 397-406
62. Wittmann BC, Schott BH, Guderian S, et al. Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron. 2005 ; 45: 459-467
63. Zierhut K, Bogerts B, Schott B, et al. The role of hippocampus dysfunction in deficient memory encoding and positive symptoms in schizophrenia. Psychiatry Res. 2010 ; 183: 187-194