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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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BackgroundAcute effect of isometric exercise on desire to smoke and tobacco withdrawal symptoms
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“In such cue reactivity studies it was repeatedly demonstrated that craving can reliably be induced by appropriate cues (see Carter and Tiffany, 1999, for a meta-analytic review).”
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Detected, selected, and sometimes neglected: cognitive processing of cues in addiction.
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“It is possible that circadian changes in craving were triggered by environmental stimuli that have a strong impact on craving and smoking behavior (Carter and Tiffany 1999).”
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“…cues are repeatedly paired with positively and/or negatively reinforcing drug effects (e.g., Baker, Piper, McCarthy, Majeskie, & Fiore, 2004; Carter & Tiffany, 1999); however, such conceptualizations fail to account for the ambivalence that substance abusers commonly display toward the…”
BackgroundThe urge to smoke depends on the expectation of smoking
Dols, M., van den Hout, M., Kindt, M., & Willems, B. (2002) · Addiction · doi:10.1046/j.1360-0443.2002.00010.x · Cited by 80
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“VR induces craving for alcohol with effect sizes typically 2 SD in magnitude (Bordnick et al., 2008); three times the effect size found in traditional non-VR cue exposure alcohol craving research (Carter & Tiffany, 1999a; Carter & Tiffany, 1999b).”
BackgroundGenetic influences on craving for alcohol
Arpana Agrawal, A., Wetherill, L. F., Bucholz, K. K., Kramer, J., Samuel Kuperman, C., Lynskey, M. T., Nürnberger, J. I., Schuckit, M. A., Tischfield, J. A., Edenberg, H. J., et al. (2012) · Addictive Behaviors · doi:10.1016/j.addbeh.2012.03.021 · Cited by 80
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“In substance dependency research, cue reactivity has been described as a result of repeated drug use in which learning mechanisms lead to an association of internal or environmental cues with the reinforcing effects of a drug.(19) As a consequence of classical conditioning, formerly neutral cues become conditioned, pr…”
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“…(eg, heart rate), subjective (eg, craving), appetitive approach behaviors (eg, drug-seeking), and activation of specific corticostriatal subcircuits elicited by conditioned stimuli associated with motivationally salient events (Carter and Tiffany, 1999; Field and Cox, 2008; Koob and Volkow, 2010).”
A meta-analysis of cue reactivity in tobacco cigarette smokers
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“…rise to feelings of craving, and although early evidence suggested that these cravings were infrequent in addicts and often unrelated to drug use (Carter & Tiffany, 1999; Tiffany & Conklin, 2000), more recent studies using ecological momentary assessment techniques (used to capture behavior in…”
ResultEffect of impulsivity on craving and behavioral reactivity to smoking cues
Doran, N., Spring, B. J., & McChargue, D. E. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0832-x · Cited by 81
“18 reported in a recent meta-analysis (Carter and Tiffany 1999), suggesting somewhat limited potency of the cue manipulation.”
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Brain Activation During Craving for Alcohol Measured by Positron Emission Tomography
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“In the SPECT study, a traditional cue-exposure design was used which had been established in numerous studies, investigating selfreports of craving and various vegetative psychophysiological parameters in response to alcohol-related cues [5,20].”
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“In their meta-analysis, Carter and Tiffany (1999) found that increases in selfreported craving and changes in autonomic functioning are reliably evoked when smokers are exposed to tobaccorelated stimuli compared with neutral stimuli.”
Horrell, T., El-Baz, A. S., Baruth, J. M., Tasman, A., Sokhadze, G. E., Stewart, C., & Sokhadze, E. M. (2010) · Journal of Neurotherapy · doi:10.1080/10874208.2010.501498 · Cited by 76
“…responses to stimuli associated with the preferred substance of abuse (alcohol, nicotine, cocaine, heroin, etc.) is relatively well explored (Carter & Tiffany, 1999; Childress et al., 1999; Drummond, Tiffany, Gautier, & Remington, 1995; Ehrman et al., 1998; Lubman, Peters, Mogg, Bradley, &…”
InfluentialGrounding desire and motivated behavior: A theoretical framework and review of empirical evidence
Papies, E. K., & Barsalou, L. W. (2015) · Utrecht University Repository (Utrecht University) · Cited by 77
Location and longing: The nicotine craving experience in virtual reality
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Self-citationReactivity to nicotine cues over repeated cue reactivity sessions
LaRowe, S. D., Saladin, M. E., Carpenter, M. J., & Upadhyaya, H. P. (2007) · Addictive Behaviors · doi:10.1016/j.addbeh.2007.04.025 · Cited by 72
“Measures of craving and cue reactivity have been used within the field of addictions research to predict relapse in drug-dependent individuals as well as assess the efficacy of novel pharmacological agents for the treatment of addictions (Carter & Tiffany, 1999; Modesto-Lowe & Kranzler, 1999).”
MethodPornographic Picture Processing Interferes with Working Memory Performance
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Validation of smoking-related virtual environments for cue exposure therapy
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“Moreover, in spite of the recognized importance of CSs for tobacco and heroin dependence (Rohsenow et al. 1990; Carter and Tiffany 1999; Hogarth et al. 2006) and of the known DA-stimulant properties of nicotine and opiates (Di Chiara 2002), no information is available on the ability of these drugs…”
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“…laboratory animals (See, 2002; Shaham et al., 2003; Stewart et al., 2000; Weiss, 2005) can be triggered by conditions reported to provoke drug craving and relapse in human such as a drug (de Wit, 1996), drug-associated cues (Carter & Tiffany, 1999; Childress et al., 1993), or stress (Sinha, 2001).”
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“significantly greater subjective craving responses than did water beverage cues, with effect sizes comparable to previous studies (Cooney et al. 1997; Carter and Tiffany 1999).”
InfluentialAccounting for the Social Triggers of Sexual Compulsivity
Parsons, J. T., Kelly, B. C., Bimbi, D. S., Muench, F. J., & Morgenstern, J. (2007) · Journal of Addictive Diseases · doi:10.1300/j069v26n03_02 · Cited by 73
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“Withdrawal is often manifested through a decrease in heart rate and skin conductance during drug cue exposure ( Carter & Tiffany, 1999 ; Niaura et al., 1988 ).”
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Transdiagnostic Connectome-Based Prediction of Craving
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“…by methylphenidate, a dopamine agonist and stimulant, suggest the impact on results of the following factors: (A) heightened arousal/autonomic reactions (Carter and Tiffany, 1999; Ehrman, et al., 1992; Glautier and Drummond, 1994; Margolin, et al., 1994; Sinha, et al., 2000); (B) ‘fresher’…”
Cognitive Regulation of Craving in Alcohol‐Dependent and Social Drinkers
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“Although the specific role of cue-induced craving in compulsive drinking and relapse is a matter of debate (Tiffany and Conklin, 2000), cue-induced craving is a widely studied laboratory phenomenon, associated with a well-characterized set of subjective, behavioral, autonomic, and neural responses (Carter and Tiffany,…”
The cerebellum in drug craving
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“Drug addicts are presented with drug-related cues under abstinence, while both craving levels and neurobiological parameters are evaluated (Carter and Tiffany, 1999).”
BackgroundWang, L., Wu, L., Wang, Y., Li, H., Liu, X., Du, X., & Dong, G. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.01150 · Cited by 77
“…by addiction-related cues (Blumenthal and Gold, 2009), which is thought to play a critical role in developing and maintaining addictive behaviors (Carter and Tiffany, 1999; Tong et al., 2007; Goudriaan et al., 2010), as well as relapse to addictive behaviors (Cooney et al., 1997; Kosten et al.,…”
BackgroundContext-induced relapse after extinction versus punishment: similarities and differences
Marchant, N. J., Campbell, E. J., Pelloux, Y., Bossert, J. M., & Shaham, Y. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4929-1 · Cited by 70
“…finding from these studies is that most human drug users relapse to drug use when they return to their home environment after successful extinction of the physiological and psychological responses to drugassociated discrete cues in the clinic (Carter and Tiffany 1999; Conklin and Tiffany 2002).”
BackgroundWilson, S. J., Creswell, K. G., Sayette, M. A., & Fiez, J. A. (2012) · Addictive Behaviors · doi:10.1016/j.addbeh.2012.03.020 · Cited by 68
“…which could affect the content, and all legal disclaimers that apply to the journal pertain. ark-text $w aterm ark-text $w aterm ark-text Cigarette smokers exhibit a variety of affective, cognitive, and physiological responses when presented with smoking-related stimuli (Carter & Tiffany, 1999).”
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“Relapse may be triggered by a variety of events including exposure to drug-related cues (Carter and Tiffany, 1999) or stress (Sinha, 2001).”
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“Because self-reported urge is the most common index of craving across studies and has shown the most powerful effects (Carter & Tiffany, 1999), we focus on this measure.”
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“2) (Carter and Tiffany 1999), making it difficult to identify the factors responsible for these effects.”
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BackgroundNeural correlates of cue reactivity in individuals with smartphone addiction
Schmitgen, M. M., Horvath, J., Mundinger, C., Wolf, N. D., Sambataro, F., Hirjak, D., Kubera, K. M., Koenig, J., & Wolf, R. C. (2020) · Addictive Behaviors · doi:10.1016/j.addbeh.2020.106422 · Cited by 74
Pretreatment cue reactivity predicts end-of-treatment smoking
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“…of factors have been shown to impact reactivity parameters, including type of cue, nicotine deprivation, mood, nicotine dependence, and gender (Carter & Tiffany, 1999; Niaura et al., 1998; Payne, Schare, Levis, & Colletti, 1991; Payne, Smith, Sturges, & Holleran, 1996; Tiffany & Drobes, 1990).”
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“Alcohol-related images in cue–reactivity studies have been found to increase craving or urges to drink in heavy alcohol users compared to ‘neutral’ or control cues [69,70,66,67,71].”
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“C ONDITIONED CUES ASSOCIATED with alcohol can induce craving in humans (Carter and Tiffany, 1999), which results in alcohol-seeking and consumption (e.”
BackgroundAssociation of Neural Responses to Drug Cues With Subsequent Relapse to Stimulant Use
MacNiven, K. H., Jensen, E. L. S., Borg, N., Padula, C. B., Humphreys, K. N., & Knutson, B. D. (2018) · JAMA Network Open · doi:10.1001/jamanetworkopen.2018.6466 · Cited by 63
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BackgroundThe Cambridge Handbook of Substance and Behavioral Addictions
Sussman, S. Y. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108632591 · Cited by 64
Amlung, M. T., McCarty, K. N., Morris, D. H., Tsai, C., & McCarthy, D. M. (2015) · Addiction · doi:10.1111/add.12897 · Cited by 63
“Both of these manipulations commonly elicit increases in craving [27, 28].”
BackgroundDunbar, M. S., Scharf, D., Kirchner, T., & Shiffman, S. (2010) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntp198 · Cited by 64
Warthen, M. W., & Tiffany, S. T. (2009) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0015617 · Cited by 64
“P A A uthor M anuscript cravings for alcohol, cocaine, heroin, marijuana, and tobacco (Bauer & Kranzler, 1994; Carter & Tiffany, 1999; Conklin & Tiffany, 2001; Drobes & Tiffany, 1997; Sell et al., 2000; Singleton, Trotman, & Zavahir, Taylor, & Heishman, 2002; Sinha et al., 2003; Streeter et al.,…”
BackgroundResultSelf-citationMartinović, J., Jones, A., Christiansen, P., Rose, A. K., Hogarth, L., & Field, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094605 · Cited by 62
Cue Reactivity in Active Pathological, Abstinent Pathological, and Regular Gamblers
Sodano, R., & Wulfert, E. (2009) · Journal of Gambling Studies · doi:10.1007/s10899-009-9146-8 · Cited by 64
“This paradigm has proven useful in studying basic theoretical issues related to our understanding of addictive behaviors (Drummond et al. 1995; Carter and Tiffany 1999).”
Avoidance of smoking: the impact of warning labels in Brazil
Nascimento, B. E. M., Oliveira, L., Vieira, A. S., Joffily, M., Gleiser, S., Pereira, M. G., Cavalcante, T., & Volchan, E. (2008) · Tobacco Control · doi:10.1136/tc.2008.025643 · Cited by 64
Filip, M., & Frankowska, M. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.05.069 · Cited by 63
Wilson, S. J., Sayette, M. A., & Fiez, J. A. (2011) · Journal of Abnormal Psychology · doi:10.1037/a0025112 · Cited by 62
“Finally, while several studies have demonstrated that smoking cues robustly increase the urge to smoke (Carter & Tiffany, 1999), the design of the current experiment (i.e., the fixed order of cues) leaves open the possibility that observed increases in self-reported craving were attributable in…”
BackgroundVentral Tegmental Area Afferents and Drug-Dependent Behaviors
Oliva, I., & Wanat, M. J. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00030 · Cited by 68
Alvarez‐Jaimes, L., Polis, I. Y., & Parsons, L. H. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301630 · Cited by 64
“Self-reports by drug-dependent humans indicate that multiple factors such as exposure to drug-associated stimuli, drug priming, and stress can precipitate drug craving and relapse (Jaffe et al, 1989; O’Brien et al, 1992; Kreek and Koob, 1998; Carter and Tiffany, 1999; Sinha et al, 1999).”
BackgroundReed, D. D., Kaplan, B. A., Roma, P. G., & Hursh, S. R. (2014) · The Psychological Record · doi:10.1007/s40732-014-0076-1 · Cited by 62
Ferguson, S. G., & Shiffman, S. S. (2010) · Substance Use & Misuse · doi:10.3109/10826084.2011.521399 · Cited by 61
“Drug dependence has traditionally been investigated using either highly focused laboratory studies (e.g., cue reactivity studies; Carter & Tiffany, 1999) or observational or epidemiological study designs.”
MethodDeconstructing Craving: Dissociable Cortical Control of Cue Reactivity in Nicotine Addiction
Scott, D., & Hiroi, N. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.01.023 · Cited by 71
“All groups of mice consumed indistinguishable amounts of nicotine (Group, F(3,27) = 0.”
BackgroundSituations and moods associated with smoking in everyday life.
Shapiro, D., Jamner, L. D., Davydov, D. M., & James, P. (2002) · Psychology of Addictive Behaviors · doi:10.1037//0893-164x.16.4.342 · Cited by 66
Kandasamy, A., & Menon, J. (2018) · Indian Journal of Psychiatry · doi:10.4103/psychiatry.indianjpsychiatry_36_18 · Cited by 69
Kareken, D. A., Liang, T., Wetherill, L. F., Džemidžić, M., Bragulat, V., Cox, C., Talavage, T. M., O’Connor, S., & Foroud, T. (2010) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01293.x · Cited by 63
“Such Pavlovian “conditioned stimuli” are thought to be important in the maintenance of drinking, craving, and relapse (Carter & Tiffany, 1999; Cooney et al., 1997; Litt et al., 2000; Cox et al., 2002).”
BackgroundLiu, X., Jernigen, C., Gharib, M. A., Booth, S., Caggiula, A. R., & Sved, A. F. (2010) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e328337be95 · Cited by 61
“…factor critically contributing to the resumption of drug use in abstinent addicts is the exposure to environmental stimuli associated earlier with drug intake (Stewart et al., 1984; Niaura et al., 1989; Childress et al., 1993; Drummond et al., 1995; O’Brien et al., 1998; Carter and Tiffany, 1999).”
BackgroundNIAURA, R. S., Sayette, M. A., Shiffman, S. S., Glover, E. D., Nides, M., Shelanski, M. V., Shadel, W. G., Koslo, R., Robbins, B., & Sorrentino, J. (2005) · Addiction · doi:10.1111/j.1360-0443.2005.01218.x · Cited by 61
Laier, C., & Brand, M. (2014) · Sexual Addiction & Compulsivity · doi:10.1080/10720162.2014.970722 · Cited by 62
“Therefore, cue-reactivity and craving are substantial mechanisms of the development and maintenance of addiction; furthermore, they are associated with relapse (Carter & Tiffany, 1999; Tiffany & Wray, 2012).”
BackgroundStippekohl, B., Winkler, M. H., Mucha, R. F., Pauli, P., Walter, B., Vaitl, D., & Stark, R. M. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.227 · Cited by 64
“It is well known that drug availability plays an important role in the modulation of cue-reactivity (Wertz and Sayette, 2001; Carter and Tiffany, 2001; Wilson et al, 2004, McBride et al, 2006). Furthermore, Mucha et al (2008) suggested that the perceived smoke availability is an important factor for the differential r…”
BackgroundEffects of Systematic Cue Exposure Through Virtual Reality on Cigarette Craving
Pericot‐Valverde, I., Secades‐Villa, R., Gutiérrez‐Maldonado, J., & García–Rodríguez, O. (2014) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntu104 · Cited by 61
Intraadministration associations: Conditional hyperalgesia elicited by morphine onset cues.
Sokolowska, M., Siegel, S., & Kim, J. A. (2002) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.28.3.309 · Cited by 61
“If addicts' responses to drug-related stimuli reflect CRs, then extinction of these CRs may be achieved through repeated unreinforced exposure to the CS " (Carter & Tiffany, 1999, p. 329).”
BackgroundMoors, A. (2017) · Psychological Inquiry · doi:10.1080/1047840x.2017.1235900 · Cited by 70
Addiction Research Unit: Affective and cognitive mechanisms of specific Internet‐use disorders
Brand, M., Müller, A., Stark, R. M., Steins‐Loeber, S., Klucken, T., Montag, C., Diers, M., Wolf, O. T., Rumpf, H., Wölfling, K., et al. (2021) · Addiction Biology · doi:10.1111/adb.13087 · Cited by 64
Peak provoked craving: an alternative to smoking cue‐reactivity
Sayette, M. A., & Tiffany, S. T. (2012) · Addiction · doi:10.1111/j.1360-0443.2012.04013.x · Cited by 60
Self-citationKim, A. E., Nonnemaker, J. M., Loomis, B. R., Shafer, P. R., Shaikh, A., Hill, E., Holloway, J. W., & Farrelly, M. C. (2014) · American Journal of Public Health · doi:10.2105/ajph.2013.301723 · Cited by 60
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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