Altered neural processing of the need to stop in young adults at risk for stimulant dependence

Journal of Neuroscience

Volumn 34, Issue 13, 2014, Pages 4567-4580

  Harlé, Katia M ^a   Shenoy, Pradeep ^b   Stewart, Jennifer L ^a   Tapert, Susan F ^a,c   Yu, Angela J ^b   Paulus, Martin P ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Bayesian model; Cognitive control; Ideal observer model; Inhibitory control; Stimulants

Indexed keywords

CANNABIS; COCAINE;

ANTERIOR CINGULATE; ARTICLE; BAYES THEOREM; BEHAVIOR; BOLD SIGNAL; CONTROLLED STUDY; CORRELATION COEFFICIENT; DRUG DEPENDENCE; DRUG USE; DSM-IV; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE ANALYSIS; MALE; NERVE CELL; NERVOUS SYSTEM PARAMETERS; NEURAL PROCESSING; PARAHIPPOCAMPAL GYRUS; PREDICTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; QUESTIONNAIRE; REACTION TIME; SCORING SYSTEM; SIGNAL TRANSDUCTION;

BAYESIAN MODEL; COGNITIVE CONTROL; IDEAL OBSERVER MODEL; INHIBITORY CONTROL; STIMULANTS;

BAYES THEOREM; BRAIN; BRAIN MAPPING; CHOICE BEHAVIOR; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INHIBITION (PSYCHOLOGY); LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; OXYGEN; REACTION TIME; RISK; SUBSTANCE-RELATED DISORDERS; YOUNG ADULT;

EID: 84897892094     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2297-13.2014     Document Type: Article

References (81)

1. Aarts E, Roelofs A (2011) Attentional control in anterior cingulate cortex based on probabilistic cueing. J Cogn Neurosci 23:716-727. CrossRef Medline
2. Arikuni T, Watanabe K, Kubota K (1988) Connections of area 8 with area 6 in the brain of the macaque monkey. J Comp Neurol 277:21-40. CrossRef Medline
3. Aron AR, Poldrack RA (2006) Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 26:2424-2433. CrossRef Medline
4. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW (2003) Stopsignal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115-116. CrossRef Medline
5. Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170-177. CrossRef Medline
6. Aron JL, Paulus MP (2007) Location, location: using functional magnetic resonance imaging to pinpoint brain differences relevant to stimulant use. Addiction 102:33-43. CrossRef Medline
7. Barratt ES (1959) Anxiety and impulsiveness related to psychomotor efficiency. Perceptual and Motor Skills 9:191-198. CrossRef
8. Behrens TE, Woolrich MW, Walton ME, Rushworth MF (2007) Learning the value of information in an uncertain world. Nat Neurosci 10:1214-1221. CrossRef Medline
9. Bolla KI, Eldreth DA, London ED, Kiehl KA, Mouratidis M, Contoreggi C, Matochik JA, Kurian V, Cadet JL, Kimes AS, Funderburk FR, Ernst M (2003) Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task. Neuroimage 19:1085-1094. CrossRef Medline
10. Bolla K, Ernst M, Kiehl K, Mouratidis M, Eldreth D, Contoreggi C, Matochik J, Kurian V, Cadet J, Kimes A, Funderburk F, London E (2004) Prefrontal cortical dysfunction in abstinent cocaine abusers. J Neuropsychiatry Clin Neurosci 16:456-464. CrossRef Medline
11. Bossaerts P (2010) Risk and risk prediction error signals in anterior insula. Brain Struct Funct 214:645-653. CrossRef Medline
12. Büchel C, Holmes AP, Rees G, Friston KJ (1998) Characterizing stimulus-response functions using nonlinear regressors in parametric f MRI experiments. Neuroimage 8:140-148. CrossRef Medline
13. Bucholz KK, Cadoret R, Cloninger CR, Dinwiddie SH, Hesselbrock VM, Nurnberger JI Jr, Reich T, Schmidt I, Schuckit MA (1994) A new, semistructured psychiatric interview for use in genetic linkage studies: a report on the reliability of the SSAGA. J Stud Alcohol 55:149-158. Medline
14. Cauda F, D'Agata F, Sacco K, Duca S, Geminiani G, Vercelli A (2011) Functional connectivity of the insula in the resting brain. Neuroimage 55:8-23. CrossRef Medline
15. Chambers CD, Bellgrove MA, Stokes MG, Henderson TR, Garavan H, Robertson IH, Morris AP, Mattingley JB (2006) Executive "brake failure" following deactivation of human frontal lobe. J Cogn Neurosci 18:444-455. CrossRef Medline
16. Clark VP, Beatty GK, Anderson RE, Kodituwakku P, Phillips JP, Lane TDR, Kiehl KA, Calhoun VD (2012) Reduced f MRI activity predicts relapse in patients recovering from stimulant dependence. Hum Brain Mapp.
17. Cloninger CR (1986) A unified biosocial theory of personality and its role in the development of anxiety states. Psychiatr Dev 4:167-226. Medline
18. Cloninger CR, Przybeck TR, Svrakic DM, Wetzel RD (1994) The Temperament and Character Inventory (TCI): a guide to its development and use. St. Louis: Center for Psychobiology of Personality, Washington University.
19. Colzato LS, van den Wildenberg WPM, Hommel B (2007) Impaired inhibitory control in recreational cocaine users. PLo S One 2:e1143. CrossRef Medline
20. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162-173. CrossRef Medline
21. Di Martino A, Scheres A, Margulies DS, Kelly AM, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP (2008) Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 18:2735-2747. CrossRef Medline
22. Elkashef A, Vocci F (2003) Biological markers of cocaine addiction: implications for medications development. Addict Biol 8:123-139. CrossRef Medline
23. Emeric EE, Brown JW, Boucher L, Carpenter RH, Hanes DP, Harris R, Logan GD, Mashru RN, Paré M, Pouget P, Stuphorn V, Taylor TL, Schall JD. (2007) Influence of history on saccade countermanding performance in humans and macaque monkeys. Vis Res 47:35-49. CrossRef Medline
24. Euston DR, Gruber AJ, McNaughton BL (2012) The role of medial prefrontal cortex in memory and decision making. Neuron 76:1057-1070. CrossRef Medline
25. Fillmore MT, Rush CR (2002) Impaired inhibitory control of behavior in chronic cocaine users. Drug Alcohol Depend 66:265-273. CrossRef Medline
26. Fu LP, Bi GH, Zou ZT, Wang Y, Ye EM, Ma L, Ming-Fan, Yang Z (2008) Impaired response inhibition function in abstinent heroin dependents: an f MRI study. Neurosci Lett 438:322-326. CrossRef Medline
27. Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652-669. CrossRef Medline
28. Hanes DP, Schall JD (1995) Countermanding saccades in macaque. Vis Neurosci 12:929-937. Medline
29. Hayden BY, Heilbronner SR, Pearson JM, Platt ML (2011) Surprise signals in anterior cingulate cortex: neuronal encoding of unsigned reward prediction errors driving adjustment in behavior. J Neurosci 31:4178-4187. CrossRef Medline
30. Hester R, Garavan H (2004) Executive dysfunction in cocaine addiction: evidence for discordant frontal, cingulate, and cerebellar activity. J Neurosci 24:11017-11022. CrossRef Medline
31. Hester R, Simões-Franklin C, Garavan H (2007) Post-error behavior in active cocaine users: poor awareness of errors in the presence of intact performance adjustments. Neuropsychopharmacology 32:1974-1984. CrossRef Medline
32. Ide JS, Shenoy P, Yu AJ, Li CS (2013) Bayesian prediction and evaluation in the anterior cingulate cortex. J Neurosci 33:2039-2047. CrossRef Medline
33. Kaufman JN, Ross TJ, Stein EA, Garavan H (2003) Cingulate hypoactivity in cocaine users during a GO-NOGO task as revealed by event-related functional magnetic resonance imaging. J Neurosci 23:7839-7843. Medline
34. Kemmotsu N, Villalobos ME, Gaffrey MS, Courchesne E, Müller RA (2005) Activity and functional connectivity of inferior frontal cortex associated with response conflict. Brain Res Cogn Brain Res 24:335-342. CrossRef Medline
35. Kennerley SW, Behrens TE, Wallis JD (2011) Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nat Neurosci 14:1581-1589. CrossRef Medline
36. Kim YT, Lee SW, Kwon DH, Seo JH, Ahn BC, Lee J (2009) Dose-dependent frontal hypometabolism on FDG-PET in methamphetamine abusers. J Psychiatr Res 43:1166-1170. CrossRef Medline
37. Lawrence AJ, Luty J, Bogdan NA, Sahakian BJ, Clark L (2009) Impulsivity and response inhibition in alcohol dependence and problem gambling. Psychopharmacology 207:163-172. CrossRef Medline
38. Li CS, Huang C, Constable RT, Sinha R (2006) Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing. J Neurosci 26:186-192. CrossRef Medline
39. Li CS, Huang C, Yan P, Bhagwagar Z, Milivojevic V, Sinha R (2008) Neural correlates of impulse control during stop signal inhibition in cocainedependent men. Neuropsychopharmacology 33:1798-1806. CrossRef Medline
40. Logan GD, Cowan WB (1984) On the ability to inhibit thought and action: A theory of an act of control. Psychol Rev 91:295. CrossRef
41. London ED, Simon SL, Berman SM, Mandelkern MA, Lichtman AM, Bramen J, Shinn AK, Miotto K, Learn J, Dong Y, Matochik JA, Kurian V, Newton T, Woods R, Rawson R, Ling W (2004) Mood disturbances and regional cerebral metabolic abnormalities in recently abstinent methamphetamine abusers. Arch Gen Psychiatry 61:73-84. CrossRef Medline
42. Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2007) Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37:579-588. CrossRef Medline
43. Matthews SC, Simmons AN, Arce E, Paulus MP (2005) Dissociation of inhibition from error processing using a parametric inhibitory task during functional magnetic resonance imaging. Neuroreport 16:755-760. CrossRef Medline
44. Monterosso JR, Aron AR, Cordova X, Xu J, London ED (2005) Deficits in response inhibition associated with chronic methamphetamine abuse. Drug Alcohol Depend 79:273-277. CrossRef Medline
45. Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G, Jones PB, Bullmore ET, Robbins TW, Fletcher PC (2008) Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry 13:239, 267-276. CrossRef Medline
46. O'Doherty JP (2004) Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol 14:769-776. CrossRef Medline
47. O'Reilly JX, Schüffelgen U, Cuell SF, Behrens TE, Mars RB, Rushworth MF (2013) Dissociable effects of surprise and model update in parietal and anterior cingulate cortex. Proc Natl Acad Sci U S A 110:E3660-E3669. CrossRef Medline
48. Paré M, Hanes DP (2003) Controlled movement processing: superior colliculus activity associated with countermanded saccades. J Neurosci 23: 6480-6489. Medline
49. Paulus MP, Hozack N, Frank L, Brown GG, Schuckit MA (2003) Decision making by methamphetamine-dependent subjects is associated with error-rate-independent decrease in prefrontal and parietal activation. Biol Psychiatry 53:65-74. CrossRef Medline
50. Paulus MP, Tapert SF, Schuckit MA (2005) Neural activation patterns of methamphetamine-dependent subjects during decision making predict relapse. Arch Gen Psychiatry 62:761-768. CrossRef Medline
51. Paulus MP, Lovero KL, Wittmann M, Leland DS (2008) Reduced behavioral and neural activation in stimulant users to different error rates during decision making. Biol Psychiatry 63:1054-1060. CrossRef Medline
52. Pinheiro J, Bates D, Deb Roy S, Sarkar D (2011) The RDevelopment Core Team 2011 nlme: linear and nonlinear mixed effects models. R package version 3.1-102. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://cran.r-project.org/web/packages/nlme/index.html.
53. Preuschoff K, Quartz SR, Bossaerts P (2008) Human insula activation reflects risk prediction errors as well as risk. J Neurosci 28:2745-2752. CrossRef Medline
54. Reske M, Delis DC, Paulus MP (2011) Evidence for subtle verbal fluency deficits in occasional stimulant users: quick to play loose with verbal rules. J Psychiatr Res 45:361-368. CrossRef Medline
55. Ridderinkhof KR, van den Wildenberg WP, Segalowitz SJ, Carter CS (2004) Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn 56:129-140. CrossRef Medline
56. Rushworth MF, Behrens TE (2008) Choice, uncertainty and value in prefrontal and cingulate cortex. Nat Neurosci 11:389-397. CrossRef Medline
57. Salo R, Nordahl TE, Possin K, Leamon M, Gibson DR, Galloway GP, Flynn NM, Henik A, Pfefferbaum A, Sullivan EV (2002) Preliminary evidence of reduced cognitive inhibition in methamphetamine-dependent individuals. Psychiatry Res 111:65-74. CrossRef Medline
58. Scangos KW, Stuphorn V (2010) Medial frontal cortex motivates but does not control movement initiation in the countermanding task. J Neurosci 30:1968-1982. CrossRef Medline
59. Schall JD, Stuphorn V, Brown JW (2002) Monitoring and control of action by the frontal lobes. Neuron 36:309-322. CrossRef Medline
60. Seo H, Lee D (2007) Temporal filtering of reward signals in the dorsal anterior cingulate cortex during a mixed-strategy game. J Neurosci 27:8366-8377. CrossRef Medline
61. Shenoy P, Yu AJ (2011) Rational decision-making in inhibitory control. Front Hum Neurosci 5.
62. Shenoy P, Rao RPN, Yu A (2011) A rational decision making framework for inhibitory control. Adv Neural Inf Process Syst 24.
63. Simon SL, Domier CP, Sim T, Richardson K, Rawson RA, Ling W (2002) Cognitive performance of current methamphetamine and cocaine abusers. J Addict Dis 21:61-74. CrossRef Medline
64. Singer T, Critchley HD, Preuschoff K (2009) A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 13:334-340. CrossRef Medline
65. Somerville LH, Heatherton TF, Kelley WM (2006) Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nat Neurosci 9:1007-1008. CrossRef Medline
66. Stewart JL, Flagan TM, May AC, Reske M, Simmons AN, Paulus MP (2013) Young adults at risk for stimulant dependence show reward dysfunction during reinforcement-based decision making. Biol Psychiatry 73:235-241. CrossRef Medline
67. Stuphorn V, Schall JD (2006) Executive control of countermanding saccades by the supplementary eye field. Nat Neurosci 9:925-931. CrossRef Medline
68. Stuphorn V, Brown JW, Schall JD (2010) Role of supplementary eye field in saccade initiation: executive, not direct, control. J Neurophysiol 103:801-816. CrossRef Medline
69. Sugiura M, Kawashima R, Nakagawa M, Okada K, Sato T, Goto R, Sato K, Ono S, Schormann T, Zilles K, Fukuda H (2000) Correlation between human personality and neural activity in cerebral cortex. Neuroimage 11:541-546. CrossRef Medline
70. Tabibnia G, Monterosso JR, Baicy K, Aron AR, Poldrack RA, Chakrapani S, Lee B, London ED (2011) Different forms of self-control share a neurocognitive substrate. J Neurosci 31:4805-4810. CrossRef Medline
71. Tapert SF, Granholm E, Leedy NG, Brown SA (2002) Substance use and withdrawal: neuropsychological functioning over 8 years in youth. J Int Neuropsychol Soc 8:873-883. Medline
72. Verbruggen F, Logan GD (2009) Models of response inhibition in the stopsignal and stop-change paradigms. Neurosci Biobehav Rev 33:647-661. CrossRef Medline
73. Verdejo-García AJ, López-Torrecillas F, Aguilar de Arcos F, Perez-Garcia M (2005) Differential effects of MDMA, cocaine, and cannabis use severity on distinctive components of the executive functions in polysubstance users: a multiple regression analysis. Addict Behav 30:89-101. CrossRef Medline
74. Volkow ND, Fowler JS, Wang GJ (1999) Imaging studies on the role of dopamine in cocaine reinforcement and addiction in humans. J Psychopharmacol 13:337-345. CrossRef Medline
75. Wechsler D (2001) Wechsler Test of Adult Reading: WTAR: Psychological Corporation.
76. White NM (1997) Mnemonic functions of the basal ganglia. Curr Opin Neurobiol 7:164-169. CrossRef Medline
77. Yoshida W, Ishii S (2006) Resolution of uncertainty in prefrontal cortex. Neuron 50:781-789. CrossRef Medline
78. Yu A, Cohen J (2009) Sequential effects: Superstition or rational behavior. Advances in Neural Information Processing Systems 21:1873-1880.
79. Yu AJ, Dayan P (2005) Uncertainty, neuromodulation, and attention. Neuron 46:681-692. CrossRef Medline
80. Zago L, Petit L, Turbelin MR, Andersson F, Vigneau M, Tzourio-Mazoyer N (2008) How verbal and spatial manipulation networks contribute to calculation: an f MRI study. Neuropsychologia 46:2403-2414. CrossRef Medline
81. Zuckerman M, Link K (1968) Construct validity for the sensation-seeking scale. J Consult Clin Psychol 32:420-426. CrossRef Medline