Susceptibility to interference between Pavlovian and instrumental control is associated with early hazardous alcohol use.
Pavlovian-to-instrumental transfer
high-risk drinking
interference control
Journal
Addiction biology
ISSN: 1369-1600
Titre abrégé: Addict Biol
Pays: United States
ID NLM: 9604935
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
31
08
2020
received:
04
03
2020
accepted:
09
10
2020
pubmed:
24
11
2020
medline:
15
12
2021
entrez:
23
11
2020
Statut:
ppublish
Résumé
Pavlovian-to-instrumental transfer (PIT) tasks examine the influence of Pavlovian stimuli on ongoing instrumental behaviour. Previous studies reported associations between a strong PIT effect, high-risk drinking and alcohol use disorder. This study investigated whether susceptibility to interference between Pavlovian and instrumental control is linked to risky alcohol use in a community sample of 18-year-old male adults. Participants (N = 191) were instructed to 'collect good shells' and 'leave bad shells' during the presentation of appetitive (monetary reward), aversive (monetary loss) or neutral Pavlovian stimuli. We compared instrumental error rates (ER) and functional magnetic resonance imaging (fMRI) brain responses between the congruent and incongruent conditions, as well as among high-risk and low-risk drinking groups. On average, individuals showed a substantial PIT effect, that is, increased ER when Pavlovian cues and instrumental stimuli were in conflict compared with congruent trials. Neural PIT correlates were found in the ventral striatum and the dorsomedial and lateral prefrontal cortices (lPFC). Importantly, high-risk drinking was associated with a stronger behavioural PIT effect, a decreased lPFC response and an increased neural response in the ventral striatum on the trend level. Moreover, high-risk drinkers showed weaker connectivity from the ventral striatum to the lPFC during incongruent trials. Our study links interference during PIT to drinking behaviour in healthy, young adults. High-risk drinkers showed higher susceptibility to Pavlovian cues, especially when they conflicted with instrumental behaviour, indicating lower interference control abilities. Increased activity in the ventral striatum (bottom-up), decreased lPFC response (top-down), and their altered interplay may contribute to poor interference control in the high-risk drinkers.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12983Informations de copyright
© 2020 The Authors. Addiction Biology published by John Wiley & Sons Ltd on behalf of Society for the Study of Addiction.
Références
Cartoni E, Balleine B, Baldassarre G. Appetitive Pavlovian-instrumental transfer: a review. Neurosci Biobehav Rev. 2016;71:829-848.
Holmes NM, Marchand AR, Coutureau E. Pavlovian to instrumental transfer: a neurobehavioural perspective. Neurosci Biobehav Rev. 2010;34(8):1277-1295.
Allman MJ, DeLeon IG, Cataldo MF, Holland PC, Johnson AW. Learning processes affecting human decision making: an assessment of reinforcer-selective Pavlovian-to-instrumental transfer following reinforcer devaluation. J Exp Psychol Anim Behav Process. 2010;36(3):402-408.
Eder AB, Dignath D. Asymmetrical effects of posttraining outcome revaluation on outcome-selective Pavlovian-to-instrumental transfer of control in human adults. Learn Motiv. 2016;54:12-21.
Paredes-Olay C, Abad MJ, Gamez M, Rosas JM. Transfer of control between causal predictive judgments and instrumental responding. Anim Learn Behav. 2002;30(3):239-248.
Quail SL, Morris RW, Balleine BW. Stress associated changes in Pavlovian-instrumental transfer in humans. Q J Exp Psychol (Hove). 2017;70(4):675-685.
Rosas JM, Paredes-Olay MC, García-Gutiérrez A, Espinosa JJ, Abad MJ. Outcome-specific transfer between predictive and instrumental learning is unaffected by extinction but reversed by counterconditioning in human participants. Learn Motiv. 2010;41:48-66.
Watson P, Wiers RW, Hommel B, de Wit S. Working for food you don't desire. Cues interfere with goal-directed food-seeking. Appetite. 2014;79:139-148.
Eder AB, Dignath D. Cue-elicited food seeking is eliminated with aversive outcomes following outcome devaluation. Q J Exp Psychol (Hove). 2016;69(3):574-588.
Huys QJM, Cools R, Golzer M, et al. Disentangling the roles of approach, activation and valence in instrumental and Pavlovian responding. PLoS Comput Biol. 2011;7(4):e1002028.
Geurts DE, Huys QJ, den Ouden HE, Cools R. Aversive Pavlovian control of instrumental behavior in humans. J Cogn Neurosci. 2013;25(9):1428-1441.
Lewis AH, Niznikiewicz MA, Delamater AR, Delgado MR. Avoidance-based human Pavlovian-to-instrumental transfer. Eur J Neurosci. 2013;38(12):3740-3748.
Nadler N, Delgado MR, Delamater AR. Pavlovian to instrumental transfer of control in a human learning task. Emotion. 2011;11(5):1112-1123.
Garofalo S, Robbins TW. Triggering Avoidance: Dissociable Influences of Aversive Pavlovian Conditioned Stimuli on Human Instrumental Behavior. Front Behav Neurosci. 2017;11:63.
Sommer C, Garbusow M, Junger E, et al. Strong seduction: impulsivity and the impact of contextual cues on instrumental behavior in alcohol dependence. Transl Psychiatry. 2017;7(8):e1183.
Freeman SM, Alvernaz D, Tonnesen A, Linderman D, Aron AR. Suppressing a motivationally-triggered action tendency engages a response control mechanism that prevents future provocation. Neuropsychologia. 2015;68:218-231.
Cavanagh JF, Eisenberg I, Guitart-Masip M, Huys Q, Frank MJ. Frontal theta overrides Pavlovian learning biases. J Neurosci. 2013;33(19):8541-8548.
Garbusow M, Schad DJ, Sebold M, et al. Pavlovian-to-instrumental transfer effects in the nucleus accumbens relate to relapse in alcohol dependence. Addict Biol. 2016;21(3):719-731.
Garbusow M, Schad DJ, Sommer C, et al. Pavlovian-to-instrumental transfer in alcohol dependence: a pilot study. Neuropsychobiology. 2014;70(2):111-121.
Schad DJ, Garbusow M, Friedel E. Neural correlates of instrumental responding in the context of alcohol-related cues index disorder severity and relapse risk. Eur Arch Psychiatry Clin Neurosci. 2019;269 (3):295-308.
Garbusow M, Nebe S, Sommer C, et al. Pavlovian-to-instrumental transfer and alcohol consumption in young male social drinkers: behavioral, neural and polygenic correlates. J Clin Med. 2019;8(8):1188.
Sommer C, Birkenstock J, Garbusow M, et al. Dysfunctional approach behavior triggered by alcohol-unrelated Pavlovian cues predicts long-term relapse in alcohol dependence. Addict Biol. 2018;25(1):e12703.
Mendelsohn A, Pine A, Schiller D. Between thoughts and actions: motivationally salient cues invigorate mental action in the human brain. Neuron. 2014;81(1):207-217.
Prevost C, Liljeholm M, Tyszka JM, O'Doherty JP. Neural correlates of specific and general Pavlovian-to-instrumental transfer within human amygdalar subregions: a high-resolution fMRI study. J Neurosci. 2012;32(24):8383-8390.
Talmi D, Seymour B, Dayan P, Dolan RJ. Human pavlovian-instrumental transfer. J Neurosci. 2008;28(2):360-368.
Bray S, Rangel A, Shimojo S, Balleine B, O'Doherty JP. The neural mechanisms underlying the influence of Pavlovian cues on human decision making. J Neurosci. 2008;28(22):5861-5866.
Hung Y, Gaillard SL, Yarmak P, Arsalidou M. Dissociations of cognitive inhibition, response inhibition, and emotional interference: Voxelwise ALE meta-analyses of fMRI studies. Hum Brain Mapp. 2018;39(10):4065-4082.
Jacobi F, Mack S, Gerschler A, et al. The design and methods of the mental health module in the German Health Interview and Examination Survey for Adults (DEGS1-MH). Int J Methods Psychiatr Res. 2013;22(2):83-99.
Wittchen H-U, Pfister H. DIA-X-Interviews: Manual für Screening-Verfahren und Interview; Interviewheft. Frankfurt: Swets Test Services; 1997.
Saß H, Wittchen H-U, Zaudig M, Houben I. DSM-IV-TR-Diagnostisches und Statistisches Manual Psychischer Störungen-Textrevision. Göttingen: Hogrefe; 2003.
Stockwell T, Chikritzhs T, Dawson D. International guide for monitoring alcohol consumption and related harm. Geneva, Switzerland: World Health Organization; 2000.
Gorgolewski K, Burns CD, Madison C, et al. Nipype: a flexible, lightweight and extensible neuroimaging data processing framework in python. Front Neuroinform. 2011;5:13.
Liu X, Hairston J, Schrier M, Fan J. Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev. 2011;35(5):1219-1236.
Friston KJ, Harrison L, Penny W. Dynamic causal modelling. Neuroimage. 2003;19(4):1273-1302.
Penny WD, Stephan KE, Daunizeau J. Comparing Families of Dynamic Causal Models. PLoS Comput Biol. 2010;6(3):e1000709.
Stephan KE, Penny WD, Moran RJ, den Ouden HE, Daunizeau J, Friston KJ. Ten simple rules for dynamic causal modeling. Neuroimage. 2010;49(4):3099-3109.
Corbit LH, Janak PH, Balleine BW. General and outcome-specific forms of Pavlovian-instrumental transfer: the effect of shifts in motivational state and inactivation of the ventral tegmental area. Eur J Neurosci. 2007;26(11):3141-3149.
Murschall A, Hauber W. Inactivation of the ventral tegmental area abolished the general excitatory influence of Pavlovian cues on instrumental performance. Learn Mem. 2006;13(2):123-126.
Domenech P, Koechlin E. Executive control and decision-making in the prefrontal cortex. Curr Opin Behav Sci. 2015;1:101-106.
Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S. The role of the medial frontal cortex in cognitive control. Science. 2004;306(5695):443-447.
Egner T, Hirsch J. Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information. Nat Neurosci. 2005;8(12):1784-1790.
Kouneiher F, Charron S, Koechlin E. Motivation and cognitive control in the human prefrontal cortex. Nat Neurosci. 2009;12(7):939-945.
Amodio DM, Frith CD. Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci. 2006;7(4):268-277.
Haber SN. Corticostriatal circuitry. Neuroscience in the 21st Century 2016:1-21.
Peters SK, Dunlop K, Downar J. Cortico-striatal-thalamic loop circuits of the salience network: a central pathway in psychiatric disease and treatment. Front Syst Neurosci. 2016;10:104.
Freeman SM, Razhas I, Aron AR. Top-down response suppression mitigates action tendencies triggered by a motivating stimulus. Curr Biol. 2014;24(2):212-216.
Carbia C, Lopez-Caneda E, Corral M, Cadaveira F. A systematic review of neuropsychological studies involving young binge drinkers. Neurosci Biobehav Rev. 2018;90:332-349.
MacLeod CM. The Stroop task: the “gold standard” of attentional measures. J Exp Psychol Gen. 1992;121(1):12-14.
Stroop JR. Studies of interference in serial verbal reactions. J Exp Psychol. 1935;18(6):643-662.
Simon JR, Rudell AP. Auditory SR compatibility: the effect of an irrelevant cue on information processing. J Appl Psychol. 1967;51(3):300-304.
Hommel B. The Simon effect as tool and heuristic. Acta Psychol (Amst). 2011;136(2):189-202.
Heinz A, Kiefer F, Smolka MN, et al. Addiction research consortium: losing and regaining control over drug intake (ReCoDe)-from trajectories to mechanisms and interventions. Addict Biol. 2020;25(2):e12866.