Manipulation of nicotinic acetylcholine receptors differentially affects behavioral inhibition in human subjects with and without disordered baseline impulsivity

Psychopharmacology

Volumn 220, Issue 2, 2012, Pages 331-340

  Potter, Alexandra S ^a   Bucci, David J ^b   Newhouse, Paul A ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b Dartmouth College   (United States)

Author keywords

Acetylcholine; ADHD; Behavioral inhibition; Cholinergic; Impulsivity; Mecamylamine; Nicotine; Reaction time; Stop signal task

Indexed keywords

MECAMYLAMINE; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; PLACEBO;

ADULT; ARTICLE; BEHAVIORAL SCIENCE; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; FEMALE; HUMAN; HUMAN EXPERIMENT; IMPULSIVENESS; MALE; NEUROMODULATION; PRIORITY JOURNAL; PROTEIN FUNCTION; RANDOMIZED CONTROLLED TRIAL; RESPONSE TIME; SIGNAL DETECTION; SIGNAL PROCESSING; TASK PERFORMANCE;

ADMINISTRATION, CUTANEOUS; ADOLESCENT; CHOICE BEHAVIOR; DOUBLE-BLIND METHOD; FEMALE; HUMANS; IMPULSIVE BEHAVIOR; INHIBITION (PSYCHOLOGY); MALE; MECAMYLAMINE; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; REACTION TIME; RECEPTORS, NICOTINIC; YOUNG ADULT;

EID: 84858442425     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2476-0     Document Type: Article

References (80)

1. Aron AR, Poldrack RA (2006) Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 26:2424-2433 (Pubitemid 44699002)
2. Aron AR, Dowson JH, Sahakian BJ, Robbins TW (2003) Methylphenidate improves response inhibition in adults with attention-deficit/hyperactivity disorder. Biol Psychiatr 54:1465-1468 (Pubitemid 37522172)
3. Aron AR, Durston S, Eagle DM, Logan GD, Stinear CM, Stuphorn V (2007) Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition. J Neurosci 27:11860-11864 (Pubitemid 350072098)
4. Balint S, Czobor P, Komlosi S, Meszaros A, Simon V, Bitter I (2009) Attention deficit hyperactivity disorder (ADHD): gender- and age-related differences in neurocognition. Psychol Med 39:1337-1345
5. Band GP, van der Molen MW, Logan GD (2003) Horse-race model simulations of the stop-signal procedure. Acta Psychol (Amst) 112:105-142 (Pubitemid 36881099)
6. Bari A, Eagle DM, Mar AC, Robinson ES, Robbins TW (2009) Dissociable effects of noradrenaline, dopamine, and serotonin uptake blockade on stop task performance in rats. Psychophar-macol (Berl) 205:273-283
7. Barkley R (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121(1):65-94 (Pubitemid 127705285)
8. Bates T, Pellett O, Stough C, Mangan G (1994) Effects of smoking on simple and choice reaction time. Psychopharmacol (Berl) 114:365-368 (Pubitemid 24152129)
9. Bedard AC, Nichols S, Barbosa JA, Schachar R, Logan GD, Tannock R (2002) The development of selective inhibitory control across the life span. Dev Neuropsychol 21:93-111 (Pubitemid 34568634)
10. Bedard AC, Ickowicz A, Logan GD, Hogg-Johnson S, Schachar R, Tannock R (2003) Selective inhibition in children with attention-deficit hyperactivity disorder off and on stimulant medication. J Abnorm Child Psychol 31:315-327 (Pubitemid 36626755)
11. Biederman J, Mick E, Faraone S, Hammerness P, Surman C, Harpold T, Dougherty M, Aleardi M, Spencer T (2006) A double-blind comparison of galantamine hydrogen bromide and placebo in adults with attention-deficit/ hyperactivity disorder: a pilot study. J Clin Psychopharmacol 26:163-166 (Pubitemid 43740340)
12. Boonstra AM, Kooij JJ, Oosterlaan J, Sergeant JA, Buitelaar JK (2005) Does methylphenidate improve inhibition and other cognitive abilities in adults with childhood-onset ADHD? J Clin Exp Neuropsychol 27:278-298 (Pubitemid 40523416)
13. Bucci DJ, Holland PC, Gallagher M (1998) Removal of cholinergic input to rat posterior parietal cortex disrupts incremental processing of conditioned stimuli. J Neurosci 18:8038-8046 (Pubitemid 28441041)
14. Bymaster FP, Katner JS, Nelson DL, Hemrick-Luecke SK, Threlkeld PG, Heiligenstein JH, Morin SM, Gehlert DR, Perry KW (2002) Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsycho-pharmacol 27:699-711 (Pubitemid 35335888)
15. Chamberlain SR, Muller U, Blackwell AD, Clark L, Robbins TW, Sahakian BJ (2006) Neurochemical modulation of response inhibition and probabilistic learning in humans. Science 311:861-863 (Pubitemid 43228852)
16. Chamberlain SR, Hampshire A, Muller U, Rubia K, Del Campo N, Craig K, Regenthal R, Suckling J, Roiser JP, Grant JE, Bullmore ET, Robbins TW, Sahakian BJ (2009) Atomoxetine modulates right inferior frontal activation during inhibitory control: a pharmacological functional magnetic resonance imaging study. Biol Psychiatry 65:550-555
17. Chiba AA, Bucci DJ, Holland PC, Gallagher M (1995) Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing. J Neurosci 15:7315-7322
18. Cohen J (1977) Statistical power analysis for behavioral sciences (revised ed.). Academic Press, New York
19. Conners CK, Levin ED, Sparrow E, Hinton SC, Erhardt D, Meck WH, Rose JE, March J (1996) Nicotine and attention in adult attention deficit hyperactivity disorder (ADHD). Psychopharma-col Bull 32:67-73 (Pubitemid 26176204)
20. De Jong R, Coles MG, Logan GD, Gratton G (1990) In search of the point of no return: the control of response processes. J Exp Psychol Hum Percept Perform 16:164-182
21. De Jong R, Coles MG, Logan GD (1995) Strategies and mechanisms in nonselective and selective inhibitory motor control. J Exp Psychol Hum Percept Perform 21:498-511
22. de Wit H, Crean J, Richards JB (2000) Effects of d-amphetamine and ethanol on a measure of behavioral inhibition in humans. Behav Neurosci 114:830-837 (Pubitemid 30646572)
23. DeVito EE, Blackwell AD, Clark L, Kent L, Dezsery AM, Turner DC, Aitken MR, Sahakian BJ (2009) Methylphenidate improves response inhibition but not reflection-impulsivity in children with attention deficit hyperactivity disorder (ADHD). Psycho-pharmacol (Berl) 202:531-539
24. Dews PB (1977) Rate-dependency hypothesis. Science 198:1182-1183
25. Dumas JA, Saykin AJ, McDonald BC, McAllister TW, Hynes ML, Newhouse PA (2008) Nicotinic versus muscarinic blockade alters verbal working memory-related brain activity in older women. Am J Geriatr Psychiatr 16:272-282
26. Eagle DM, Lehmann O, Theobald DE, Pena Y, Zakaria R, Ghosh R, Dalley JW, Robbins TW (2009) Serotonin depletion impairs waiting but not stop-signal reaction time in rats: implications for theories of the role of 5-HT in behavioral inhibition. Neuro-psychopharmacol 34:1311-1321
27. Fillmore MT, Rush CR (2002) Impaired inhibitory control of behavior in chronic cocaine users. Drug Alcohol Depend 66:265-273 (Pubitemid 34327862)
28. First MB, Spitzer RL, Gibbon M, Williams J (1996) Structured Clinical Interview for DSM-IV Axis I Disorders-Patient Edition @CID-I/P, Version 2.0. New York State Psychiatric Institute, New York
29. Fischer M, Barkley RA, Smallish L, Fletcher K (2007) Hyperactive children as young adults: driving abilities, safe driving behavior, and adverse driving outcomes. Accid Anal Prev 39:94-105 (Pubitemid 44633822)
30. Gehricke JG, Loughlin SE, Whalen CK, Potkin SG, Fallon JH, Jamner LD, Belluzzi JD, Leslie FM (2007) Smoking to self-medicate attentional and emotional dysfunctions. Nicotine Tob Res 9 (Suppl 4):S523-S536
31. Gehricke JG, Hong N, Whalen CK, Steinhoff K, Wigal TL (2009) Effects of transdermal nicotine on symptoms, moods, and cardiovascular activity in the everyday lives of smokers and nonsmokers with attention-deficit/hyperactivity disorder. Psychol Addict Behav 23:644-655
32. Hindmarch I (1984) Psychological performance models as indicators of the effects of hypnotic drugs on sleep. Psychopharmacology Suppl 1:58-68
33. Horner WE, Johnson DE, Schmidt AW, Rollema H (2007) Methyl-phenidate and atomoxetine increase histamine release in rat prefrontal cortex. Eur J Pharmacol 558:96-97 (Pubitemid 46328877)
34. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N (1997) Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data [see comment]. J Am Acad Child Adolesc Psychiatr 36:980-988 (Pubitemid 27272932)
35. Kerr JS, Sherwood N, Hindmarch I (1991) Separate and combined effects of the social drugs on psychomotor performance. Psychopharmacol (Berl) 104:113-119
36. Kollins SH, McClernon FJ, Fuemmeler BF (2005) Association between smoking and attention-deficit/hyperactivity disorder symptoms in a population-based sample of young adults. Arch Gen Psychiatr 62:1142-1147 (Pubitemid 41396939)
37. Lambert NM, Hartsough CS, Sassone D, Sandoval J (1987) Persistence of hyperactivity symptoms from childhood to adolescence and associated outcomes. Am J Orthopsychiatr 57:22-32 (Pubitemid 17124488)
38. Levin ED, Conners CK, Sparrow E, Hinton SC, Erhardt D, Meck WH, Rose JE, March J (1996) Nicotine effects on adults with attention-deficit/hyperactivity disorder. Psychopharmacol (Berl) 123:55-63
39. Levin ED, Conners CK, Silva D, Hinton SC, Meck WH, March J, Rose JE (1998) Transdermal nicotine effects on attention. Psychopharmacol (Berl) 140:135-141 (Pubitemid 28538472)
40. Levin ED, McClernon FJ, Rezvani AH (2006) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacol 184:523-539 (Pubitemid 43255869)
41. Logan GD (1994) On the ability to inhibit thought and action: a users guide to the stop signal paradigm. In: Dagenbach D, Carr TH (eds) Inhibitory processes in attention, memory and language. Academic, San Diego
42. Logan GD, Cowan WB, Davis KA (1984) On the ability to inhibit simple and choice reaction time responses: a model and a method. J Exp Psychol Hum Percept Perform 10:276-291
43. Mancuso G, Lejeune M, Ansseau M (2001) Cigarette smoking and attention: processing speed or specific effects? Psychopharma-colo 155:372-378 (Pubitemid 32523107)
44. Mansvelder HD, McGehee DS (2002) Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 53:606-617 (Pubitemid 35375590)
45. McNair DM, Lorr M, Droppleman LF (1971) Manual for the profile of mood states. Educational and Industrial Testing Service, San Diego
46. Mick E, Biederman J, Faraone SV, Sayer J, Kleinman S (2002) Case-control study of attention-deficit hyperactivity disorder and maternal smoking, alcohol use, and drug use during pregnancy. J Am Acad Child Adolesc Psychiatr 41:378-385 (Pubitemid 38327913)
47. Milberger S, Faraone SV, Biederman J, Chu MP, Wilens T (1998) Familial risk analysis of the association between attention-deficit/hyperactivity disorder and psychoactive substance use disorders. Arch Pediatr Adolesc Med 152:945-951
48. Monterosso JR, Aron AR, Cordova X, Xu J, London ED (2005) Deficits in response inhibition associated with chronic metham-phetamine abuse. Drug Alcohol Depend 79:273-277 (Pubitemid 40942119)
49. Morris SB, DeShon RP (2002) Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. Psychol Methods 7:105-125
50. Newhouse P, Potter A, Corwin J, Lenox R (1994) Age-related effects of the nicotinic antagonist mecamylamine on cognition and behavior. Neuropsychopharmacology, 10: 93-107 (Pubitemid 24152360)
51. Oosterlaan J, Sergeant JA (1998) Response inhibition and response reengagement in attention-deficit/hyperactivity disorder, disruptive, anxious and normal children. Behavioural brain research 94:33-43 (Pubitemid 28352462)
52. Overtoom CC, Verbaten MN, Kemner C, Kenemans JL, van Engeland H, Buitelaar JK, van der Molen MW, van der Gugten J, Westenberg H, Maes RA, Koelega HS (2003) Effects of methylphenidate, desipramine, and L-dopa on attention and inhibition in children with attention deficit hyperactivity disorder. Behav Brain Res 145:7-15 (Pubitemid 37188627)
53. Perkins KA (1999) Baseline-dependency of nicotine effects: a review. Behav Pharmacol 10:597-615 (Pubitemid 30026054)
54. Picciotto MR (2003) Nicotine as a modulator of behavior: beyond the inverted U. Trends Pharmacol Sci 24:493-499 (Pubitemid 37088175)
55. Pomerleau OF, Downey KK, Stelson FW, Pomerleau CS (1995) Cigarette smoking in adult patients diagnosed with attention deficit hyperactivity disorder. J Subst Abuse 7:373-378 (Pubitemid 26032582)
56. Potter AS, Newhouse PA (2004) Effects of acute nicotine administration on behavioral inhibition in adolescents with attention-deficit/hyperactivity disorder. Psychopharmacol (Berl) 176:182-194 (Pubitemid 39517948)
57. Potter AS, Newhouse PA (2008) Acute nicotine improves cognitive deficits in young adults with attention-deficit/hyperactivity disorder. Pharmacol Biochem Behav 88:407-417 (Pubitemid 350266783)
58. Potter AS, Newhouse PA, Bucci DJ (2006) Central nicotinic cholinergic systems: a role in the cognitive dysfunction in attention-deficit/hyperactivity disorder? Behav Brain Res 175:201-211 (Pubitemid 44750245)
59. Quik M, Jeyarasasingam G (2000) Nicotinic receptors and Parkinson's disease. Eur J Pharmacol 393:223-230 (Pubitemid 30193420)
60. Robinson ES, Eagle DM, Mar AC, Bari A, Banerjee G, Jiang X, Dalley JW, Robbins TW (2008) Similar effects of the selective noradrenaline reuptake inhibitor atomoxetine on three distinct forms of impulsivity in the rat. Neuropsychopharmacol 33:1028-1037 (Pubitemid 351367544)
61. Rubia K, Smith AB, Brammer MJ, Toone B, Taylor E (2005) Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. Am J Psychiatry 162:1067-1075 (Pubitemid 40770688)
62. Sarter M, Bruno JP, Givens B (2003) Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory? Neurobiol Learning Memory 80:245-256 (Pubitemid 37159352)
63. Sarter M, Hasselmo ME, Bruno JP, Givens B (2005) Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res-Brain Res Rev 48:98-111 (Pubitemid 40215784)
64. Sarter M, Parikh V, Howe WM (2009a) nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem Pharmacol 78:658-667
65. Sarter M, Parikh V, Howe WM (2009b) Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat Rev Neurosci 10:383-390
66. Schmitz M, Denardin D, Laufer Silva T, Pianca T, Hutz MH, Faraone S, Rohde LA (2006) Smoking during pregnancy and attention-deficit/hyperactivity disorder, predominantly inattentive type: a case-control study. J Am Acad Child Adolesc Psychiatry 45:1338-1345 (Pubitemid 44665451)
67. Sherwood N, Kerr JS, Hindmarch I (1992) Psychomotor performance in smokers following single and repeated doses of nicotine gum. Psychopharmacol (Berl) 108:432-436
68. Shytle RD, Silver AA, Wilkinson BJ, Sanberg PR (2002) A pilot controlled trial of transdermal nicotine in the treatment of attention deficit hyperactivity disorder. World J Biol Psychiatr 3:150-155
69. Singh A, Potter A, Newhouse P (2004) Nicotinic acetylcholine receptor system and neuropsychiatric disorders. IDrugs 7:1096-1103 (Pubitemid 40123635)
70. Tannock R (1998) Attention deficit hyperactivity disorder: advances in cognitive, neurobiological, and genetic research. J Child Psychol Psychiatr Allied Disc 39:65-99 (Pubitemid 28059670)
71. Tzavara ET, Bymaster FP, Overshiner CD, Davis RJ, Perry KW, Wolff M, McKinzie DL, Witkin JM, Nomikos GG (2006) Procholiner-gic and memory enhancing properties of the selective norepi-nephrine uptake inhibitor atomoxetine. Mol Psychiatry 11:187-195 (Pubitemid 43164620)
72. Van Kammen DP, Murphy DL (1975) Attenuation of the euphoriant and activating effects of D- and D-amphetamine by lithium carbonate treatment. Psychopharmacol 44:215-224
73. Verbruggen F, Logan GD (2008) Response inhibition in the stop-signal paradigm. Trends Cogn Sci 12:418-424
74. Vogel-Sprott M, Easdon C, Fillmore M, Finn P, Justus A (2001) Alcohol and behavioral control: cognitive and neural mechanisms. Alcohol Clin Exp Res 25:117-121 (Pubitemid 32147702)
75. Wechsler DS (1999) Wechsler Abbreviated Scales of Intelligence. The Psychological Corporation, New York
76. Wilens TE, Biederman J, Spencer TJ, Bostic J, Prince J, Monuteaux MC, Soriano J, Fine C, Abrams A, Rater M, Polisner D (1999) A pilot controlled clinical trial of ABT-418, a cholinergic agonist, in the treatment of adults with attention deficit hyperactivity disorder. Am J Psychiatry 156:1931-1937
77. Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF (2005) Validity of the executive function theory of attention-deficit/hyperac-tivity disorder: a meta-analytic review. Biol Psychiatry 57:1336-1346 (Pubitemid 40798553)
78. Williams BR, Ponesse JS, Schachar RJ, Logan GD, Tannock R (1999) Development of inhibitory control across the life span. Development Psychol 35:205-213
79. Winstanley CA, Theobald DE, Dalley JW, Cardinal RN, Robbins TW (2006) Double dissociation between serotonergic and dopaminergic modulation of medial prefrontal and orbito-frontal cortex during a test of impulsive choice. Cereb Cortex 16:106-114 (Pubitemid 41746734)
80. Wonnacott S (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci 20:92-98 (Pubitemid 27050704)