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Meta‐analysis of cue‐reactivity in addiction research
Abstract
Aims. The cue‐reactivity procedure exposes addicts to a variety of drug‐related stimuli while self‐report of craving and physiological responses are monitored. The present review sought to determine the magnitude and overall pattern of responses typically found in cue‐reactivity research and which, if any, learning‐based model of cue reactivity is best supported by the findings. Design. Meta‐analytical techniques were used to select and evaluate results from 41 cue‐reactivity studies that compared responses of alcoholics, cigarette smokers, cocaine addicts or heroin addicts to drug‐related versus neutral stimuli. Effect sizes were calculated, separately by addict type, for self‐report of craving and physiological responses (heart rate, sweat gland activity and skin temperature). Findings. Across all addict groups, the effect size for craving was +0.92. Alcoholics had a significantly smaller craving effect size (+0.53) compared to other addict groups (+1.18 to +1.29). Relatively smaller effect sizes were found for physiological responses. The general profile of effect sizes across all addict groups was increased heart rate (+0.26) and sweat gland activity (+0.40) and decreased skin temperature (‐0.24) when addicts were presented with drug‐related stimuli. Conclusions. The cuereactivity paradigm can produce a stable profile of significant effects and, therefore, has a number of potential applications for investigating addictive phenomena. The implications of these findings for conditioning‐based models of cue‐reactivity phenomena are discussed.
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“Cognitive behaviour therapy (CBT) is a structured, time limited, evidence based psychological therapy for a wide range of emotional and behavioural disorders, including addictive behaviours12.”
From Cognitive behavioural interventions in addictive disorders (2018) · cites this paper as [12]
In the citing paper
“The targeted-effect size was chosen based on findings from studies employing CIC paradigms for drug craving52, food cravings25,37,53,54 and internet gaming craving27, which report medium-to-large effect sizes in cue reactivity52.”
From Acute social isolation evokes midbrain craving responses similar to hunger (2020) · cites this paper as [52]
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Schiebener, J., Laier, C., & Brand, M. (2015) · Journal of Behavioral Addictions · doi:10.1556/jba.4.2015.1.5 · Cited by 69
“Conclusions about this effect can be drawn by taking the concept of cue-reactivity (see Carter & Tiffany, 1999) into account: Excessive cybersex users may be conditioned to experience or expect reward when seeing the material and this conditioned response interferes with cognitive control processes.”
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“…that exposing smokers to smoking-related cues (e.g., cigarettes, ashtrays, lighters) robustly induces craving, a phenomenon termed cue reactivity (Carter & Tiffany, 1999), and that relapse often occurs in the presence of cues (Shiffman et al., 1996), it has been suggested that perhaps increased…”
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Papachristou, H., Nederkoorn, C., Giesen, J. C. A. H., & Jansen, A. T. M. (2013) · Addictive Behaviors · doi:10.1016/j.addbeh.2013.11.027 · Cited by 58
“Consequently, they elicit a motivational state that elicits subjective (e.g., craving), physiological (e.g., heart rate changes), and behavioral reactivity (e.g., alcohol drinking) (Carter & Tiffany, 1999; Stewart, de Wit, & Eikelboom, 1984).”
BackgroundWin-Concurrent Sensory Cues Can Promote Riskier Choice
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“Responses to cue reactivity assessment were modest and lower than expected based on a prior review (Carter & Tiffany, 1999).”
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“This shows that alcohol-related stimuli have a higher salience and lead to a cognitive bias, which is also known from studies evaluating the cue reactivity effect (Carter and Tiffany 1999; Drummond 2000).”
ONE HUNDRED YEARS OF ALCOHOLISM: THE TWENTIETH CENTURY
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“The focus on cue-induced craving and the underlying learning mechanisms (Glautier et al., 1994; Carter and Tiffany, 1999) has revived the discussion on whether the disease concept of alcoholism should be replaced by a social learning perspective (Heather, 1992).”
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Conditioned craving cues elicit an automatic approach tendency
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“…reactivity’ refers to the observation that exposure to substance-related cues (such as the sight or smell of alcoholic beverages) evokes elevations in subjective craving and physiological arousal and increases the likelihood of substance use (Carter and Tiffany 1999; Veilleux and Skinner 2015).”
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“…lawfully associated with drug intake can become conditioned stimuli (Robinson & Berridge 1993) and induce both subjective and psychophysiological indicators of craving (see Drummond, Cooper & Glautier 1990; for a review, see Carter & Tiffany 1990) and increased relapse risk (Heinz et al. 2009).”
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“Of the numerous factors associated with treatment outcome, craving is considered a primary trigger for relapse.(2) Additionally, environmental stimuli (contextspecific stimuli or cues) that are repeatedly associated with cigarettes are known to promote compulsive smoking.”
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“In fact, stimulation of heart rate upon drug cue exposure has been observed in the majority of cue reactivity studies for other drugs of abuse regardless of drug class (1).”
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“Considerable research has demonstrated that smokers show increased subjective, physiological, and behavioral reactivity to salient smoking cues (see Carter & Tiffany, 1999 ).”
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Curtin, J. J., Barnett, N. P., Colby, S. M., Rohsenow, D. J., & Monti, P. M. (2005) · Journal of Studies on Alcohol · doi:10.15288/jsa.2005.66.332 · Cited by 56
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“In a recent review, Carter and Tiffany 1999 discussed the implications of the cue reactivity literature for addiction research.”
BackgroundReinstatement of Morphine‐Induced ConditionedPlace Preference in Mice by Priming Injections
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“Restructuring of Responses to Drug and Natural Reward Cues Craving as an overwhelmingly strong urge is often evoked by exposure to addiction-related cues and can trigger averse physical and physiological responses as well as the strong desire to carry out the behavior in question [52].”
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“Craving can be triggered by drug or food cues (Carter and Tiffany 1999; Childress et al. 1999; Jansen et al. 2003; Sobik et al. 2005; Epstein et al. 2009).”
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Cue reactivity in virtual reality: The role of context
Paris, M. M., Carter, B. L., Traylor, A. C., Bordnick, P. S., Day, S. X., Armsworth, M. W., & Cinciripini, P. M. (2011) · Addictive Behaviors · doi:10.1016/j.addbeh.2011.01.029 · Cited by 54
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Cognitive performance and autonomic reactivity in abstinent drug abusers and nonusers.
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“Children’s cognitive resources are concentrated largely on the 354 game and food cues thus become elaborated on an automatic level (Buijzen et al., 2010), 355 directly leading to physiological and psychological reactions (Carter & Tiffany, 1999).”
BackgroundCannabis Cue Reactivity and Craving Among Never, Infrequent and Heavy Cannabis Users
Henry, E. A., Kaye, J. T., Bryan, A. D., Hutchison, K. E., & Ito, T. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.324 · Cited by 54
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“…present with both impulsivity (Moeller et al., 2001b, 2002, 2004) and high levels of reactivity to cocaine-associated cues (O’Brien et al., 1998; Carter and Tiffany, 1999; Modesto-Lowe and Kranzler, 1999), and studies in amphetamine-treated rats suggest that impulsivity and cue reactivity may…”
BackgroundSelf-regulation and its failure: The seven deadly threats to self-regulation.
Wagner, D. D., & Heatherton, T. F. (2014) · American Psychological Association eBooks · doi:10.1037/14341-026 · Cited by 66
“Since Schachter’s early work, a large volume of research has been conducted examining the role of cues in inducing cravings and excessive consumption (for reviews, see Carter & Tiffany, 1999; Hofmann, Friese, & Wiers, 2008; Jansen, 1998; Niaura et al., 1988).”
BackgroundThe Opioid-Addicted Tetrapartite Synapse
Kruyer, A., Chioma, V. C., & Kalivas, P. W. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.05.025 · Cited by 50
“An important consequence of these adaptations is that abstinent heroin users exhibit motivational bias toward heroin-related stimuli (9, 10), and elevated cue-reactivity in humans is linked to higher self-reported craving (11).”
BackgroundThe Potent Effect of Environmental Context on Relapse to Alcohol- Seeking After Extinction
Janak, P. H. (2013) · The Open Addiction Journal · doi:10.2174/1874941001003010076 · Cited by 55
The impact of cigarette deprivation and cigarette availability on cue–reactivity in smokers
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“[3,4]), smoking-related cues [5], stressors [6,7], induction of negative affect (e.”
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Stress- and cue-induced cigarette craving: Effects of a family history of smoking
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“This phenomenon can be reliably modeled under laboratory conditions, in which smokers are exposed to smoking cues and report their craving levels (Carter & Tiffany, 1999).”
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Cue-induced Craving in Pathological Buying: Empirical Evidence and Clinical Implications
Trotzke, P., Starcke, K., Pedersen, A., & Brand, M. (2014) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000126 · Cited by 51
“One possible explanation is that physiological measurements contain a great deal of noise because they depict a wide range of physiological processes of which only a fraction is reflective for cue manipulation (18).”
BackgroundInfluentialCue-specific reactivity in experienced gamblers.
Wulfert, E., Maxson, J., & Jardin, B. (2009) · Psychology of Addictive Behaviors · doi:10.1037/a0017134 · Cited by 52
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“Cue reactivity to drug-related stimuli, including needles or injecting paraphernalia, has long been associated with relapse (Carter & Tiffany, 1999; Childress et al., 1993; Namba, Tomek, Olive, Beckmann, & Gipson, 2018).”
BackgroundThe importance of housing conditions on behavioral sensitization and tolerance to ethanol
de Araujo, N. P., Camarini, R., Formigoni, M. L. O. D. S., Carvalho, R. C., Abílio, V. C., Silva, R. H., Ricardo, V. P., Ribeiro, R. D. A., & Frussa‐Filho, R. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.07.009 · Cited by 51
Context‐dependency of cue‐elicited urge to smoke
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Acute social isolation evokes midbrain craving responses similar to hungerPreprint
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“…within the smoking sequence acquire through Pavlovian conditioning the capacity to elicit an excitatory motivational state (Om), such as physiological arousal (Carter and Tiffany 1999), akin to that elicited by the inhalation itself, which modulates S-R associations to evoke the puff response.”
BackgroundTetrodotoxin reduces cue-induced drug craving and anxiety in abstinent heroin addicts
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“Even after long periods of abstinence, heroin-dependent individuals are vulnerable to impulsive drug use when in the presence of stimuli related to previous episodes of use (Carter and Tiffany, 1999), and relapse frequently occurs (O’Brien, 1997).”
BackgroundInfluentialExamining the interrelationships between social anxiety, smoking to cope, and cigarette craving
Watson, N. L., VanderVeen, J. W., Cohen, L. M., DeMarree, K. G., & Morrell, H. E. R. (2012) · Addictive Behaviors · doi:10.1016/j.addbeh.2012.03.025 · Cited by 53
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Smoking environment cues reduce ability to resist smoking as measured by a delay to smoking task
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“This conclusion supports the general approach of numerous clinical efforts to recognize the salient environmental stimuli involved in drug abuse and to reduce their effectiveness (Carter and Tiffany, 1999; Childress et al, 1993; Drummond et al, 1995; McLellan et al, 2000; O’Brien 2001).”
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Craving e dependência química: conceito, avaliação e tratamento
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“In their metaanalytic review of 41 alcohol, nicotine, cocaine, and opiate cue reactivity studies, Carter and Tiffany (1999) reported a large effect size (i.e., .92) for craving and smaller effect sizes for physiological indices (i.e., .26 for heart rate and .24 for skin temperature).”
It's the Product: Do Risky Products Compel Attention and Elicit Arousal in Media Users?
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“Carter and Tiffany (1999) conducted a meta-analysis on cue reactivity in addiction research and found that participants showed significant increases in sweat-gland activity when exposed to drug-related compared to nondrug-related stimuli.”
BackgroundMethods of assessing craving to gamble: A narrative review.
Ashrafioun, L., & Rosenberg, H. (2011) · Psychology of Addictive Behaviors · doi:10.1037/a0026367 · Cited by 54
Older Men’s Social Integration After Prison
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“In these cases, recidivism may be facilitated by interaction with criminally engaged friends and neighbors, and/or exposure to environmental “triggers” for substance use that encourage relapse (Carter & Tiffany, 1999; Kirk, 2009, 2012).”
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“The subjective experience of craving is associated with autonomic changes (Carter & Tiffany, 1999), as well as activation in attentional, interceptive, and reward-related brain networks (Koob & Volkow, 2016; Naqvi, Gaznick, Tranel, & Bechara, 2014).”
BackgroundOlanzapine attenuates cue-elicited craving for tobacco
Hutchison, K. E., Goodworth, M.-C. R., NIAURA, R. S., Swift, R. M., Pickworth, W. B., & Sobik, L. E. (2003) · Psychopharmacology · doi:10.1007/s00213-004-1837-3 · Cited by 48
“A number of studies have indicated that exposure to smoking cues (e.g. the sight and smell of a lit cigarette) markedly increases craving for tobacco (Niaura et al. 1988, 1992, 1998; Carter and Tiffany 1999; Hutchison et al. 1999; Tiffany et al. 2000; Sayette et al. 2001).”
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Taylor, A. H., & Oliver, A. J. (2008) · Appetite · doi:10.1016/j.appet.2008.09.004 · Cited by 49
Smoking behavior in context: Where and when do people smoke?
Gucht, D. V., den Bergh, O. V., Beckers, T., & Vansteenwegen, D. (2010) · Journal of Behavior Therapy and Experimental Psychiatry · doi:10.1016/j.jbtep.2009.12.004 · Cited by 47
“Thewissen, Snijders, Havermans, van den Hout, & Jansen, 2006), but also by a wide range of proximal cues (for a review see Carter & Tiffany, 1999), both external (e.g., Niaura, Abrams, Pedraza, Monti, & Rohsenow, 1992) and internal (e.g., Conklin & Perkins, 2005).”
BackgroundDingle, G. A., Kelly, P. J., Flynn, L. M., & Baker, F. A. (2015) · The Arts in Psychotherapy · doi:10.1016/j.aip.2015.05.005 · Cited by 53
Effect of deactivation of activity patterns related to smoking cue reactivity on nicotine addiction
Bu, J., Young, K. D., Hong, W., Ma, R., Song, H., Wang, Y., Zhang, W., Hampson, M., Hendler, T., & Zhang, X. (2019) · Brain · doi:10.1093/brain/awz114 · Cited by 43
Examining the relationship between cue-induced craving and actual smoking.
Conklin, C. A., Vella, E. J., Joyce, C. J., Salkeld, R. P., Perkins, K. A., & Parzynski, C. S. (2015) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0038826 · Cited by 46
“…studies demonstrating that confrontation with smoking cues significantly increases cue-induced craving among smokers and moderately alters autonomic reactivity (see Carter & Tiffany, 1999 for review), but few demonstrating an increase in actual smoking in direct response to smoking cue exposure.”
BackgroundInfluentialCorrelates of Smoking Cessation Self-efficacy in a Community Sample of Smokers
Martinez, E., Tatum, K. L., Glass, M., Bernath, A., Ferris, D., Reynolds, P., & Schnoll, R. (2009) · Addictive Behaviours · doi:10.1016/j.addbeh.2009.09.016 · Cited by 59
In vivo versus imaginal smoking cue exposures: Is seeing believing?
Erblich, J., & Bovbjerg, D. H. (2004) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.12.3.208 · Cited by 47
Singleton, E. G., Anderson, L. M., & Heishman, S. J. (2003) · Addiction · doi:10.1046/j.1360-0443.2003.00449.x · Cited by 47
Wiers, R. W., Houben, K., Smulders, F. T. Y., Conrod, P. J., & Jones, B. T. (2006) · Handbook of Implicit Cognition and Addiction · doi:10.4135/9781412976237.n22 · Cited by 47
The Prevention and Treatment of Gambling Disorders: Some Art, Some Science
Derevensky, J. L. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108632591.024 · Cited by 45
Going beyond the individual level in self-control research
Hofmann, W. (2023) · Nature Reviews Psychology · doi:10.1038/s44159-023-00256-y · Cited by 52
“For instance, laboratory experiments 53–55 , field observations 56,57 and field experiments 58,59 show how variations in stimulus microenvironments affect the desire for and the choice and consumption of products.”
Reactivity to Alcohol Cues: Isolating the Role of Perceived Availability.
MacKillop, J., & Lisman, S. A. (2005) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.13.3.229 · Cited by 46
“…however, it is notable that availability information was confounded with substance type (nicotine vs. alcohol) and significant differences in the degree of cue reactivity have been demonstrated between these two substances in a meta-analysis of cue reactivity research (Carter & Tiffany, 1999).”
BackgroundSign-tracking to an appetitive cue predicts incubation of conditioned fear in rats
Morrow, J. D., Saunders, B. T., Maren, S., & Robinson, T. E. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.04.002 · Cited by 44
D-cycloserine to enhance extinction of cue-elicited craving for alcohol: a translational approach
MacKillop, J., Few, L. R., Stojek, M. M., Murphy, C. M., Malutinok, S. F., Johnson, F. T., Hofmann, S. G., McGeary, J. E., Swift, R. M., & Monti, P. M. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.41 · Cited by 46
Liddie, S., Anderson, K. L., Paz, A., & Itzhak, Y. (2012) · Journal of Psychopharmacology · doi:10.1177/0269881112447991 · Cited by 45
“Extinction learning by ‘exposure therapy’ is thought to be essential for the management of drug addiction (Carter and Tiffany, 1999; Powell et al., 1993; Siegel and Ramos, 2002).”
BackgroundLoxton, N. J., & Dawe, S. (2006) · Personality and Individual Differences · doi:10.1016/j.paid.2006.09.031 · Cited by 46
The effects of chronic food restriction on cue-induced heroin seeking in abstinent male rats
D’Cunha, T. M., Sedki, F., Macri, J., Casola, C., & Shalev, U. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2810-1 · Cited by 46
“In abstinent addicts, drug craving and relapse can be triggered by exposure to the self-administered drug (de Wit 1996; Meyer and Mirin 1979), drug-associated cues (Carter and Tiffany 1999; Childress et al. 1992), or stressful life events (Sinha 2001).”
Hardy, L., Mitchell, C. J., Seabrooke, T., & Hogarth, L. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4605-x · Cited by 46
“Drug cue reactivity is a central construct in addiction research, and there have been numerous attempts to elucidate the underlying learning mechanisms (e.g. Carter and Tiffany 1999).”
BackgroundShin, Y., Kim, J., Kim, M.-K., Kyeong, S.-H., Jung, Y. H., Eom, H., & Kim, E. J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0195677 · Cited by 48
Wray, J. M., Godleski, S. A., & Tiffany, S. T. (2011) · Psychology of Addictive Behaviors · doi:10.1037/a0023687 · Cited by 48
“Drug cues consistently increase craving across all major substance-use disorders (Carter & Tiffany, 1999); however, all of this research has Correspondence concerning this article should be addressed to Stephen T. Tiffany, Ph.D., Department of Psychology, Park 228, University at Buffalo, The State…”
BackgroundSelf-citationMurphy, C. M., & MacKillop, J. (2014) · Alcoholism: Clinical and Experimental Research · doi:10.1111/acer.12322 · Cited by 45
Considering the Overlap and Nonoverlap of Compulsivity, Impulsivity, and Addiction
Blum, A. W., & Grant, J. E. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108632591.038 · Cited by 44
Neurobiological Foundations of Behavioral Addictions
Vaccaro, A. G., & Potenza, M. N. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108632591.016 · Cited by 45
Pavlovian-to-Instrumental Transfer across Mental Disorders: A Review
Garbusow, M., Ebrahimi, C., Riemerschmid, C., Daldrup, L., Rothkirch, M., Chen, K., Chen, H., Belanger, M. J., Hentschel, A., Smolka, M. N., et al. (2022) · Neuropsychobiology · doi:10.1159/000525579 · Cited by 73
Laboratory-induced stress and craving among individuals with prescription opioid dependence
Back, S. E., Grös, D. F., Price, M., LaRowe, S. D., Flanagan, J. C., Brady, K. T., Davis, C., Jaconis, M., & McCauley, J. L. (2015) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2015.08.019 · Cited by 46
Metadata
- Authors
- Carter, B. L., & Tiffany, S. T.
- Affiliations
- Purdue University West Lafayette (US)
- Venue
- Addiction
- Publisher
- Wiley
- Published
- 1999-03
- Volume
- 94
- Issue
- 3
- Pages
- 327-340
- ISSN
- 0965-2140 (ISSN-L)
- 1360-0443
- OpenAlex
- W1988132969
- Cited by
- 1,638
- References
- 0
- Citations by year
- 2026: 41 · 2025: 50 · 2024: 38 · 2023: 59 · 2022: 53 · 2021: 73 · 2020: 145 · 2019: 61 · 2018: 59 · 2017: 58 · 2016: 83 · 2015: 85 · 2014: 90 · 2013: 86 · 2012: 97
- FWCI
- 16.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Addiction (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (2r01da004050-09a2)
- National Institute on Drug Abuse (R01DA04050)
- Topics
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Clinical Psychology › Gambling Behavior and Treatments
- Keywords
- cue reactivity, drug craving, alcoholism, cigarette smoking, cocaine dependence, heroin addiction, physiological responses, heart rate, sweat gland activity, skin temperature
- MeSH terms
- Adult, Cues, Female, Heart Rate, Humans, Male, Research, Skin Temperature, Sweating, Randomized Controlled Trials as Topic, Substance-Related Disorders
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