Sensorimotor gating and attentional set-shifting are improved by the μ-opioid receptor agonist morphine in healthy human volunteers

International Journal of Neuropsychopharmacology

Volumn 11, Issue 5, 2008, Pages 655-669

  Quednow, Boris B ^a,c   Csomor, Philipp A ^a   Chmiel, Joelle ^a   Beck, Thilo ^b   Vollenweider, Franz X ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Die Arbeitsgemeinschaft fur risikoarmen Umgang mit Drogen   (Switzerland)

^c UNIVERSITY HOSPITAL OF PSYCHIATRY   (Switzerland)

Author keywords

opioid receptor; Acoustic startle response; CANTAB; Morphine; Prepulse inhibition; Schizophrenia; Sensorimotor gating

Indexed keywords

MORPHINE SULFATE; PLACEBO;

ACOUSTIC REFLEX; ADULT; ALERTNESS; ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; HUMAN; HUMAN EXPERIMENT; LEARNING TEST; MALE; MEMORY; MOOD; NEUROMODULATION; NORMAL HUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SCHIZOPHRENIA; SELECTIVE ATTENTION; SENSORIMOTOR FUNCTION; SINGLE DRUG DOSE; STARTLE REFLEX;

ACOUSTIC STIMULATION; ADULT; AFFECT; ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ATTENTION; DOUBLE-BLIND METHOD; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; INHIBITION (PSYCHOLOGY); MALE; MORPHINE; NEUROPSYCHOLOGICAL TESTS; PSYCHOMETRICS; STARTLE REACTION; TIME FACTORS; VERBAL LEARNING;

EID: 46449112120     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145707008322     Document Type: Article

References (97)

1. Bloom F, Segal D, Ling N, Guillemin R (1976). Endorphins : profound behavioral effects in rats suggest new etiological factors in mental illness. Science 194, 630-632.
2. Bortolato M, Aru GN, Frau R, Orru M, Fa M, Manunta M, Puddu M, Mereu G, Gessa GL (2005). Kappa opioid receptor activation disrupts prepulse inhibition of the acoustic startle in rats. Biological Psychiatry 57, 1550-1558.
3. Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L (1978). Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15, 339-343.
4. Braff DL, Geyer MA, Swerdlow NR (2001). Human studies of prepulse inhibition of startle : normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berlin) 156, 234-258.
5. Braff DL, Grillon C, Geyer MA (1992). Gating and habituation of the startle reflex in schizophrenic patients. Archives of General Psychiatry 49, 206-215.
6. Cleeland CS, Nakamura Y, Howland EW, Morgan NR, Edwards KR, Backonja M (1996). Effects of oral morphine on cold pressor tolerance time and neuropsychological performance. Neuropsychopharmacology 15, 252-262.
7. Cohen J (1988). Statistical Power Analysis for the Behavioral Sciences Hillsdale, NJ: Lawrence Earlbaum Associates.
8. Cohen RM, Cohen MR, Weingartner H, Pickar D, Murphy DL (1983). High-dose naloxone affects task performance in normal subjects. Psychiatry Research 8, 127-136.
9. Collins SL, Faura CC, Moore RA, McQuay HJ (1998). Peak plasma concentrations after oral morphine: a systematic review. Journal of Pain and Symptom Management 16, 388-402.
10. Comfort A (1977). Morphine as an antipsychotic. Relevance of a 19th-century therapeutic fashion. Lancet 2, 448-449.
11. Derogatis LR (1977). SCL-90-R, Administration, Scoring, and Procedures Manual-I for the R(evised) Version. Baltimore : John Hopkins University School of Medicine.
12. Dias R, Robbins TW, Roberts AC (1996). Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380, 69-72.
13. Domino EF (1986). Opioid-hallucinogen interactions. Pharmacology, Biochemistry, and Behavior 24, 401-405.
14. Downes JJ, Roberts AC, Sahakian BJ, Evenden JL, Morris RG, Robbins TW (1989). Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson's disease : evidence for a specific attentional dysfunction. Neuropsychologia 27, 1329-1343.
15. Duncan E, Madonick S, Chakravorty S, Parwani A, Szilagyi S, Efferen T, Gonzenbach S, Angrist B, Rotrosen J (2001). Effects of smoking on acoustic startle and prepulse inhibition in humans. Psychopharmacology (Berlin) 156, 266-272.
16. Elliott R, McKenna PJ, Robbins TW, Sahakian BJ (1995). Neuropsychological evidence for frontostriatal dysfunction in schizophrenia. Psychological Medicine 25, 619-630.
17. Ersek M, Cherrier MM, Overman SS, Irving GA (2004). The cognitive effects of opioids. Pain Management Nursing 5, 75-93.
18. Evans WO, Smith RP (1964). Some effects of morphine and amphetamine on intellectual functions and mood. Psychopharmacologia 6, 49-56.
19. Fahrenberg J, Hampel R, Selg H (1984). Das Freiburger Persönlichkeitsinventar (FPI). Göttingen : Hogrefe.
20. Faul F, Erdfelder E, Lang A-G, Buchner A (2007). G*Power 3 : a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 39, 175-191.
21. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR (2001). Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia : a decade in review. Psychopharmacology (Berlin) 156, 117-154.
22. Gianoulakis C (2004). Endogenous opioids and addiction to alcohol and other drugs of abuse. Current Topics in Medicinal Chemistry 4, 39-50.
23. Gouzoulis-Mayfrank E, Heekeren K, Thelen B, Lindenblatt H, Kovar KA, Sass H, Geyer MA (1998). Effects of the hallucinogen psilocybin on habituation and prepulse inhibition of the startle reflex in humans. Behavioral Pharmacology 9, 561-566.
24. Graham FK (1975). Presidential Address, 1974. The more or less startling effects of weak prestimulation. Psychophysiology 12, 238-248.
25. Hanks GW, O'Neill WM, Simpson P, Wesnes K (1995). The cognitive and psychomotor effects of opioid analgesics. II. A randomized controlled trial of single doses of morphine, lorazepam and placebo in healthy subjects. European Journal of Clinical Pharmacology 48, 455-460.
26. Heaton RK (1981). The Wisconsin Card Sorting Test manual. Odessa, FL: Psychological Assessment Resources.
27. Helmstaedter C, Lendt M, Lux S (2001). VLMT - Verbaler Lern- und Merkfähigkeitstest. Göttingen : Beltz Test.
28. Hill JL, Zacny JP (2000). Comparing the subjective, psychomotor, and physiological effects of intravenous hydromorphone and morphine in healthy volunteers. Psychopharmacology (Berlin) 152, 31-39.
29. Hutton SB, Puri BK, Duncan LJ, Robbins TW, Barnes TR, Joyce EM (1998). Executive function in first-episode schizophrenia. Psychological Medicine 28, 463-473.
30. Ilyutchenok RY, Dubrovina NI (1995). Memory retrieval enhancement by kappa opioid agonist and mu, delta antagonists. Pharmacology, Biochemistry, and Behavior 52, 683-687.
31. Itoh J, Ukai M, Kameyama T (1994). Dynorphin A-(1-13) potently improves the impairment of spontaneous alternation performance induced by the mu-selective opioid receptor agonist DAMGO in mice. Journal of Pharmacology and Experimental Therapeutics 269, 15-21.
32. Jacquet YF, Marks N (1976). The C-fragment of beta-lipotropin : an endogenous neuroleptic or antipsychotogen? Science 194, 632-635.
33. Janke W, Debus G (1978). Die Eigenschaftsworterliste (EWL), Manual. Gottingen: Hogrefe.
34. Jazbec S, Pantelis C, Robbins T, Weickert T, Weinberger DR, Goldberg TE (2007). Intra-dimensional/extra-dimensional set-shifting performance in schizophrenia : impact of distractors. Schizophrenia Research 89, 339-349.
35. Johnson PI, Napier TC (1997). Morphine modulation of GABA- and glutamate-induced changes of ventral pallidal neuronal activity. Neuroscience 77, 187-197.
36. Kerr B, Hill H, Coda B, Calogero M, Chapman CR, Hunt E, Buffington V, Mackie A (1991). Concentration-related effects of morphine on cognition and motor control in human subjects. Neuropsychopharmacology 5, 157-166.
37. Khantzian EJ (1985). The self-medication hypothesis of addictive disorders : focus on heroin and cocaine dependence. American Journal of Psychiatry 142, 1259-1264.
38. Koob GF (2000). Neurobiology of addiction. Toward the development of new therapies. Annals of the New York Academy of Sciences 909, 170-185.
39. Kraepelin E (1892). Ueber die Beeinflussung einfacher psychischer Vorgänge durch einige Arzneimittel. Jena: Gustav Fischer.
40. Kumari V, Cotter PA, Checkley SA, Gray JA (1997). Effect of acute subcutaneous nicotine on prepulse inhibition of the acoustic startle reflex in healthy male non-smokers. Psychopharmacology (Berlin) 132, 389-395.
41. Kumari V, Gray JA (1999). Smoking withdrawal, nicotine dependence and prepulse inhibition of the acoustic startle reflex. Psychopharmacology (Berlin) 141, 11-15.
42. Kumari V, Soni W, Mathew VM, Sharma T (2000). Prepulse inhibition of the startle response in men with schizophrenia : effects of age of onset of illness, symptoms, and medication. Archives of General Psychiatry 57, 609-614.
43. Kumari V, Soni W, Sharma T (1999). Normalization of information processing deficits in schizophrenia with clozapine. American Journal of Psychiatry 156, 1046-1051.
44. Kumari V, Soni W, Sharma T (2002). Prepulse inhibition of the startle response in risperidone-treated patients : comparison with typical antipsychotics. Schizophrenia Research 55, 139-146.
45. Lawrence AD, Sahakian BJ, Hodges JR, Rosser AE, Lange KW, Robbins TW (1996). Executive and mnemonic functions in early Huntington's disease. Brain 119, 1633-1645.
46. Leitner DS (1989). Multisensory deficits in rats produced by acute exposure to cold swim stress. Behavioral Neuroscience 103, 151-157.
47. Leumann L, Feldon J, Vollenweider FX, Ludewig K (2002). Effects of typical and atypical antipsychotics on prepulse inhibition and latent inhibition in chronic schizophrenia. Biological Psychiatry 52, 729-739.
48. Liljequist R (1981). Codeine-induced memory changes: nature and relationship to opiate system. European Journal of Clinical Pharmacology 20, 99-107.
49. Ludewig K, Geyer MA, Vollenweider FX (2003). Deficits in prepulse inhibition and habituation in never-medicated, first-episode schizophrenia. Biological Psychiatry 54, 121-128.
50. Marek GJ (2003). Behavioral evidence for mu-opioid and 5-HT2A receptor interactions. European Journal of Pharmacology 474, 77-83.
51. Marek GJ, Aghajanian GK (1998a). 5-Hydroxytryptamine-induced excitatory postsynaptic currents in neocortical layer V pyramidal cells : suppression by mu-opiate receptor activation. Neuroscience 86, 485-497.
52. Marek GJ, Aghajanian GK (1998b). The electrophysiology of prefrontal serotonin systems: therapeutic implications for mood and psychosis. Biological Psychiatry 44, 1118-1127.
53. Marek GJ, Wright RA, Gewirtz JC, Schoepp DD (2001). A major role for thalamocortical afferents in serotonergic hallucinogen receptor function in the rat neocortex. Neuroscience 105, 379-392.
54. Martin del Campo AF, McMurray RG, Besser GM, Grossman A (1992). Effect of 12-hour infusion of naloxone on mood and cognition in normal male volunteers. Biological Psychiatry 32, 344-353.
55. McGehee DS (2006). Nicotinic and opioid receptor interactions in nicotine addiction. Molecular Interventions 6, 311-314.
56. McNally GP, Akil H (2002). Opioid peptides and their receptors : overview of function in pain modulation. In : Davis KL, Charney D, Coyle JT, Nermeroff C (Eds.) Neuropsychopharmacology : The Fifth Generation of Progress (pp. 35-46). Philadelphia: Lippincott, Williams & Wilkins.
57. Mitrovic I, Napier TC (2002). Mu and kappa opioid agonists modulate ventral tegmental area input to the ventral pallidum. European Journal of Neuroscience 15, 257-268.
58. Napier TC, Mitrovic I (1999). Opioid modulation of ventral pallidal inputs. Annals of the New York Academy of Sciences 877, 176-201.
59. O'Neill WM, Hanks GW, Simpson P, Fallon MT, Jenkins E, Wesnes K (2000). The cognitive and psychomotor effects of morphine in healthy subjects : a randomized controlled trial of repeated (four) oral doses of dextropropoxyphene, morphine, lorazepam and placebo. Pain 85, 209-215.
60. Oranje B, Van Oel CJ, Gispen-De Wied CC, Verbaten MN, Kahn RS (2002). Effects of typical and atypical antipsychotics on the prepulse inhibition of the startle reflex in patients with schizophrenia. Journal of Clinical Psychopharmacology 22, 359-365.
61. Ornstein TJ, Iddon JL, Baldacchino AM, Sahakian BJ, London M, Everitt BJ, Robbins TW (2000). Profiles of cognitive dysfunction in chronic amphetamine and heroin abusers. Neuropsychopharmacology 23, 113-126.
62. Ouagazzal AM, Jenck F, Moreau JL (2001). Drug-induced potentiation of prepulse inhibition of acoustic startle reflex in mice: a model for detecting antipsychotic activity? Psychopharmacology (Berlin) 156, 273-283.
63. Owen AM, James M, Leigh PN, Summers BA, Marsden CD, Quinn NP, Lange KW, Robbins TW (1992). Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain 115, 1727-1751.
64. Owen AM, Roberts AC, Polkey CE, Sahakian BJ, Robbins TW (1991). Extra-dimensional versus intra-dimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia 29, 993-1006.
65. Pan ZZ (1998). mu-Opposing actions of the kappa-opioid receptor. Trends in Pharmacological Sciences 19, 94-98.
66. Pantelis C, Barber FZ, Barnes TR, Nelson HE, Owen AM, Robbins TW (1999). Comparison of set-shifting ability in patients with chronic schizophrenia and frontal lobe damage. Schizophrenia Research 37, 251-270.
67. Pantelis C, Harvey CA, Plant G, Fossey E, Maruff P, Stuart GW, Brewer WJ, Nelson HE, Robbins TW, Barnes TR (2004). Relationship of behavioural and symptomatic syndromes in schizophrenia to spatial working memory and attentional set-shifting ability. Psychological Medicine 34, 693-703.
68. Parwani A, Duncan EJ, Bartlett E, Madonick SH, Efferen TR, Rajan R, Sanfilipo M, Chappell PB, Chakravorty S, Gonzenbach S, et al. (2000). Impaired prepulse inhibition of acoustic startle in schizophrenia. Biological Psychiatry 47, 662-669.
69. Postma P, Gray JA, Sharma T, Geyer M, Mehrotra R, Das M, Zachariah E, Hines M, Williams SC, Kumari V (2006). A behavioural and functional neuroimaging investigation into the effects of nicotine on sensorimotor gating in healthy subjects and persons with schizophrenia. Psychopharmacology (Berlin) 184, 589-599.
70. Quednow BB, Jessen F, Kuhn KU, Maier W, Daum I, Wagner M (2006a). Memory deficits in abstinent MDMA (ecstasy) users: neuropsychological evidence of frontal dysfunction. Journal of Psychopharmacology 20, 373-384.
71. Quednow BB, Kuhn KU, Beckmann K, Westheide J, Maier W, Wagner M (2006b). Attenuation of the prepulse inhibition of the acoustic startle response within and between sessions. Biological Psychology 71, 256-263.
72. Quednow BB, Wagner M, Westheide J, Beckmann K, Bliesener N, Maier W, Kuhn KU (2006c). Sensorimotor gating and habituation of the startle response in schizophrenic patients randomly treated with amisulpride or olanzapine. Biological Psychiatry 59, 536-545.
73. Rey A (1958). L'examen clinique en psychologie. Paris : Presse Universitaire de France.
74. Rodefer JS, Nguyen TN (2006). Naltrexone reverses age-induced cognitive deficits in rats. Neurobiology of Aging. Published online : 10 November 2006. doi :10.1016/j.neurobiolaging.2006.10.005.
75. Schmauss C, Emrich HM (1985). Dopamine and the action of opiates : a reevaluation of the dopamine hypothesis of schizophrenia. With special consideration of the role of endogenous opioids in the pathogenesis of schizophrenia. Biological Psychiatry 20, 1211-1231.
76. Shallice T (1982). Specific impairments of planning. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 298, 199-209.
77. Simmons ML, Chavkin C (1996). Endogenous opioid regulation of hippocampal function. International Review of Neurobiology 39, 145-196.
78. Sipes TE, Geyer MA (1997). DOI disrupts prepulse inhibition of startle in rats via 5-HT2A receptors in the ventral pallidum. Brain Research 761, 97-104.
79. Swerdlow NR, Braff DL, Geyer MA (1999). Cross-species studies of sensorimotor gating of the startle reflex. Annals of the New York Academy of Sciences 877, 202-216.
80. Swerdlow NR, Caine SB, Geyer MA (1991). Opiate-dopamine interactions in the neural substrates of acoustic startle gating in the rat. Progress in Neuropsychopharmacology & Biological Psychiatry 15, 415-426.
81. Swerdlow NR, Geyer MA (1998). Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophrenia Bulletin 24, 285-301.
82. Swerdlow NR, Geyer MA, Braff DL (2001). Neural circuit regulation of prepulse inhibition of startle in the rat : current knowledge and future challenges. Psychopharmacology (Berlin) 156, 194-215.
83. Swerdlow NR, Hartman PL, Auerbach PP (1997). Changes in sensorimotor inhibition across the menstrual cycle : implications for neuropsychiatric disorders. Biological Psychiatry 41, 452-460.
84. Swerdlow NR, Talledo J, Sutherland AN, Nagy D, Shoemaker JM (2006). Antipsychotic effects on prepulse inhibition in normal 'low gating' humans and rats. Neuropsychopharmacology 31, 2011-2021.
85. Terenius L, Wahlstrom A, Lindstrom LH, Widerlor E (1976). Increased CSF levels of endorphins in chronic psychosis. Neuroscience Letters 3, 157-162.
86. Ukai M, Itoh J, Kobayashi T, Shinkai N, Kameyama T (1997). Effects of the kappa-opioid dynorphin A(1-13) on learning and memory in mice. Behavioural Brain Research 83, 169-172.
87. Ukai M, Okuda A (2003). Endomorphin-1, an endogenous mu-opioid receptor agonist, improves apomorphine-induced impairment of prepulse inhibition in mice. Peptides 24, 741-744.
88. Vollenweider FX, Barro M, Csomor PA, Feldon J (2006). Clozapine enhances prepulse inhibition in healthy humans with low but not with high prepulse inhibition levels. Biological Psychiatry 60, 597-603.
89. Vollenweider FX, Csomor PA, Knappe B, Geyer MA, Quednow BB (2007). The effects of the preferential 5-HT2A agonist psilocybin on prepulse inhibition of startle in healthy human volunteers depend on interstimulus interval. Neuropsychopharmacology 32, 1876-1887.
90. Vollenweider FX, Remensberger S, Hell D, Geyer MA (1999). Opposite effects of 3,4-methylenedioxymethamphetamine (MDMA) on sensorimotor gating in rats versus healthy humans. Psychopharmacology (Berlin) 143, 365-372.
91. von Zerssen D (1971). Die Beschwerde-Liste als Test. Therapiewoche 25, 1908-1920.
92. Wagner JJ, Terman GW, Chavkin C (1993). Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 363, 451-454.
93. Waldhoer M, Bartlett SE, Whistler JL (2004). Opioid receptors. Annual Review of Biochemistry 73, 953-990.
94. Walker DJ, Zacny JP (1998). Subjective, psychomotor, and analgesic effects of oral codeine and morphine in healthy volunteers. Psychopharmacology (Berlin) 140, 191-201.
95. Weisskopf MG, Zalutsky RA, Nicoll RA (1993). The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 362, 423-427.
96. Wittchen H-U, Pfister H (1997). DIA-X-Interviews : Manual für Screening-Verfahren und Interview. Frankfurt: Swets & Zeitlinger.
97. Xi ZX, Stein EA (2002). GABAergic mechanisms of opiate reinforcement. Alcohol and Alcoholism 37, 485-494.