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THE DARK SIDE OF PRODUCT ATTACHMENT: AN FMRI STUDY OF REACTIVITY
OF USERS AND NON-USERS TO ADDICTIVE ADVERTISING CUES
SHORT ABSTRACT
The aim of this research is to explore how environmental cues – namely cigarette
advertising - affect addictive product users and non-users using the brain imaging technique
developed in neuroscience functional magnetic resonance imaging (fMRI) for cue-exposed cigarette
smokers and non-smokers.
EXTENDED ABSTRACT
Advertising is a ubiquitous and pervasive environmental cue. The average consumer, for
example, is exposed on average to three thousand ads per day (Schwartz 2004). Under normal
circumstances, consumers choose which advertising cues to attend to both consciously and nonconsciously (Bargh 2002; Grunert 1996). However for consumers, environmental cues may elicit a
unique type of response affecting decision making and driving behavior (Bernheim and Rangel
2004). The aim of this research is to explore how environmental cues affect addictive product users
and non-users using the brain imaging technique developed in neuroscience functional magnetic
resonance imaging (fMRI) for cue-exposed users and non-users.
A great deal of debate, both in the literature and among advertisers and public policy
makers, centers on how environmental cues influence people to engage in risky and addictive
behaviors (Pollay 1986; Pollay et al. 1996a). Marketers and manufacturers argue that advertising
and promotional materials offer consumers brand options and information that enhance the
consumer’s ability to make choices (Gilly and Graham 1988; Goldberg et al. 2006), while
researchers and public health officials argue that there is a strong correlation between detrimental
behavior and exposure to marketing for addictive products (Pollay 1986; Pollay et al. 1996b). There
remain unanswered questions regarding how users and non-users respond to this type of stimulus. In
addition, there are conflicting indications of how craving elicited by cues impacts cognitive
processing, including cognitive depletion leading to impulsivity outside the addictive substance
domain. Given the ongoing debate there is a need for a better understanding of the underlying
psychological and physiological mechanisms that drive the reactive response to advertising cues by
users and non-users.
The research question addressed in this research is whether environmental cues – namely
cigarette advertising – cause a reactive response in the form of increased craving in users or nonusers resulting in downstream impulsive behavior as a result of cognitive resource depletion. The
study uses functional magnetic resonance imaging (fMRI) to examine the underlying neural
response to addictive (cigarette) advertising versus non-addictive (non-cigarette) advertising in
users (smokers) and non-users (non-smokers). Brain imaging data have been collected from 10
current, daily smoker and 10 non-smokers for this study. This study was a 2 (user type: smoker vs.
non-smoker) x 2 (cue type: addictive ad cue vs. non-addictive ad cues) design using a 3T fMRI
scanner.
A long history of addiction studies demonstrates how drug cues elicit craving via reactivity
to the cue (for reviews see Carter and Tiffany 1999; Childress et al. 1993; Stritzke et al. 2004).
There has also been evidence of attentional bias toward addictive cues in users (Robinson and
Berridge 2003; Robinson and Berridge 2001; Robinson and Berridge 1993). Some studies have
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shown that this response may result in increased attentional bias and increased arousal (Bradley et
al. 2004; Drobes 2002; Johnsen et al. 1997; Mogg and Bradley 2002; Munafo et al. 2003). However
other studies have found that addictive product users, when exposed to these cues, may have an
ability to inhibit the craving response and its effects (Artiges et al. 2009; Goldstein et al. 2007a;
Stippekohl et al. 2010; Volkow and Fowler 2000; Volkow et al. 2010). On the other hand, non-users
have been shown to be largely unaffected by exposure to addictive cues (Due et al. 2002; Tapert et
al. 2003). However, research on the uptake of addictive products by new users points to evidence
that addictive product cues, such as advertising, do indeed have an effect on non-users (Altman et
al. 1996; Pierce et al. 1991). Thus there remains a debate in the literature as to whether advertising
enhances or attenuates the craving response in users and how it ultimately affects non-users.
This brain imaging data indicates neural activation of brain regions that are related to
craving and self-control in smokers and non-smokers. For example, there is differential activation in
regions associated with craving including the amygdala and the thalamus. Regions associated with
self-control including the dorsolateral prefrontal cortex and anterior cingulate cortex are also
differentially activated with significant deactivation in smokers exposed to cigarette ads. The results
show significant differential activation for non-users when exposed to addictive ad cues versus nonaddictive ad cues. In addition, the results show a different effect when users are exposed to
addictive ad cues versus non-addictive ad cues. They demonstrate that a cue reactivity response
elicits significant activation in brain regions associated with craving in both non-users and users.
There is also significant activation in regions associated with cognitive resource depletion for nonusers as a result of the increased craving activation. This may be due to the fact that non-users
underestimate the effect of this type of advertising, assuming that because they do not smoke, there
ads are not targeted directly to them. However, because these non-users have not built up the ability
to resist the tempting urge response generated by the addictive product ads, brain regions necessary
in order to resist the temptations are activated. Interestingly there is significant deactivation in brain
regions of users associated with self-control indicating inhibition of the cognitive resource depletion
possibly as a way for users to cope with stimuli that they feel is targeting towards them and an urge
response for which they feel they cannot satisfy at that moment.
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REFERENCES
Altman, D. G., D. W. Levine, R. Coeytaux, J. Slade, and R. Jaffe (1996), "Tobacco promotion and
susceptibility to tobacco use among adolescents aged 12 through 17 years in a nationally
representative sample," Am J Public Health, 86 (11), 1590-93.
Artiges, Eric, Emmanuel Ricalens, Sylvie Berthoz, Marie-Odile Krebs, Jani Penttilä, Christian
Trichard, and Jean-Luc Martinot (2009), "Exposure to smoking cues during an emotion
recognition task can modulate limbic fMRI activation in cigarette smokers," Addiction
Biology, 14 (4), 469-77.
Bærentsen, Klaus B., Hans Stødkilde-Jørgensen, Bo Sommerlund, Tue Hartmann, Johannes
Damsgaard-Madsen, Mark Fosnæs, and Anders C. Green (2010), "An investigation of brain
processes supporting meditation " Cognitive Processing, 11 (1), 57-84.
Bailey, Steffani R., Katherine C. Goedeker, and Stephen T. Tiffany (2010), "The impact of cigarette
deprivation and cigarette availability on cue reactivity in smokers," Addiction, 105 (2), 36472.
Baker, Timothy B., Elsimae Morse, and Jack E. Sherman (1986), "The motivation to use drugs: A
psychobiological analysis of urges," in Nebraska Symposium on Motivation Vol. 34.
Beauregard, Mario, Johanne Levesque, and Pierre Bourgouin (2001), "Neural Correlates of
Conscious Self-Regulation of Emotion," J. Neurosci., 21 (18), 165RC-.
Binder, J. R., J. A. Frost, T. A. Hammeke, P. S. F. Bellgowan, S. M. Rao, and R. W. Cox (1999),
"Conceptual Processing during the Conscious Resting State: A Functional MRI Study,"
Journal of Cognitive Neuroscience, 11 (1), 80-93.
Bradley, B., M. Field, K. Mogg, and J. De Houwer (2004), "Attentional and evaluative biases for
smoking cues in nicotine dependence: component processes of biases in visual orienting,"
Behavioural Pharmacology, 15, 29-36.
Brody, Arthur L., Mark A. Mandelkern, Richard E. Olmstead, Jennifer Jou, Emmanuelle Tiongson,
Valerie Allen, David Scheibal, Edythe D. London, John R. Monterosso, Stephen T. Tiffany,
Alex Korb, Joanna J. Gan, and Mark S. Cohen (2007), "Neural Substrates of Resisting
Craving During Cigarette Cue Exposure," Biological Psychiatry, 62 (6), 642-51.
Carter, Brian L. and Stephen T. Tiffany (2001), "The Cue-Availability Paradigm: The Effects of
Cigarette Availability on Cue Reactivity in Smokers," Experimental & Clinical
Psychopharmacology, 9 (2), 183-90.
---- (1999), "Meta-analysis of cue-reactivity in addiction research," Addiction, 94 (3), 327-40.
Carter, Cameron S., Todd S. Braver, Deanna M. Barch, Matthew M. Botvinick, Douglas Noll, and
Jonathan D. Cohen (1998), "Anterior Cingulate Cortex, Error Detection, and the Online
Monitoring of Performance," Science, 280 (5364), 747-49.
3
Childress, A.R., A.V. Hole, R.N. Ehrman, S.J. Robbins, A.T. McLellan, and C.P. O'Brien (1993),
"Cue reactivity and cue reactivity interventions in drug dependence," NIDA Res Monogr.,
137, 73-95.
Childress, Anna Rose, A. Thomas McLellan, and Charles P. O'Brien (1986), "Conditioned
responses in a methadone population : A comparison of laboratory, clinic, and natural
settings," Journal of Substance Abuse Treatment, 3 (3), 173-79.
Cohen, Jonathan D., Matthew Botvinick, and Cameron S. Carter (2000), "Anterior cingulate and
prefrontal cortex: who's in control?," Nat Neurosci, 3 (5), 421-23.
Critchley, H. D., R. N. Melmed, E. Featherstone, C. J. Mathias, and R. J. Dolan (2001), "Brain
activity during biofeedback relaxation: A functional neuroimaging investigation," Brain,
124 (5), 1003-12.
David, Sean P., Marcus R. Munafò, Heidi Johansen-Berg, Stephen M. Smith, Robert D. Rogers,
Paul M. Matthews, and Robert T. Walton (2005), "Ventral Striatum/Nucleus Accumbens
Activation to Smoking-Related Pictorial Cues in Smokers and Nonsmokers: A Functional
Magnetic Resonance Imaging Study," Biological Psychiatry.
Dehaene, Stanislas, Michael I. Posner, and Don M. Tucker (1994), "Localization of a Neural
System for Error Detection and Compensation," Psychological Science, 5 (5), 303-05.
Drobes, David J. (2002), "Cue Reactivity in Alcohol and Tobacco Dependence," Alcoholism:
Clinical and Experimental Research, 26 (12), 1928-29.
Due, Deborah L., Scott A. Huettel, Warren G. Hall, and David C. Rubin (2002), "Activation in
mesolimbic and visuospatial neural circuits elicited by smoking cues: Evidence from
functional magnetic resonance imaging," American Journal of Psychiatry, 159 (6), 954-60.
Ehrman, Ronald, Steven Robbins, Anna Childress, and Charles O'Brien (1992), "Conditioned
responses to cocaine-related stimuli in cocaine abuse patients," Psychopharmacology, 107
(4), 523-29.
George, Mark S., Raymond F. Anton, Courtnay Bloomer, Charlotte Teneback, David J. Drobes,
Jeffrey Lorberbaum, Ziad Nahas, and Diana J. Vincent (2001), "Activation of Prefrontal
Cortex and Anterior Thalamus in Alcoholic Subjects on Exposure to Alcohol-Specific
Cues," Arch Gen Psychiatry, 58, 345.
Gilly, Mary C. and John L. Graham (1988), "A Macroeconomic Study of the Effects of Promotion
on the Consumption of Infant Formula in Developing Countries," Journal of
Macromarketing, 8 (1), 21.
Gloria, Rebecca, Lisa Angelos, Hillary S. Schaefer, James M. Davis, Matthew Majeskie, Burke S.
Richmond, John J. Curtin, Richard J. Davidson, and Timothy B. Baker (2009), "An fMRI
investigation of the impact of withdrawal on regional brain activity during nicotine
anticipation," Psychophysiology.
4
Goldberg, Marvin E., Ronald M. Davis, and Anne Marie O'Keefe (2006), "The role of tobacco
advertising and promotion: themes employed in litigation by tobacco industry witnesses,"
Tob Control, 15 (suppl_4), iv54-67.
Goldstein, R. Z., D. Tomasi, S. Rajaram, L. A. Cottone, L. Zhang, T. Maloney, F. Telang, N. AliaKlein, and N. D. Volkow (2007a), "Role of the anterior cingulate and medial orbitofrontal
cortex in processing drug cues in cocaine addiction," Neuroscience, 144 (4), 1153-59.
Goldstein, Rita Z., Nelly Alia-Klein, Dardo Tomasi, Jean Honorio Carrillo, Thomas Maloney,
Patricia A. Woicik, Ruiliang Wang, Frank Telang, and Nora D. Volkow (2009), "Anterior
cingulate cortex hypoactivations to an emotionally salient task in cocaine addiction,"
Proceedings of the National Academy of Sciences, 106 (23), 9453-58.
Goldstein, Rita Z., Nelly Alia-Klein, Dardo Tomasi, Lei Zhang, Lisa A. Cottone, Thomas Maloney,
Frank Telang, Elisabeth C. Caparelli, Linda Chang, Thomas Ernst, Dimitris Samaras, Nancy
K. Squires, and Nora D. Volkow (2007b), "Is Decreased Prefrontal Cortical Sensitivity to
Monetary Reward Associated With Impaired Motivation and Self-Control in Cocaine
Addiction?," Am J Psychiatry, 164 (1), 43-51.
Goldstein, RZ and ND Volkow (2002), "Drug addiction and its underlying neurobiological basis:
neuroimaging evidence for the involvement of the frontal cortex," Am J Psychiatry, 159
(10), 1642-52.
Hahn, Britta, Thomas J. Ross, Yihong Yang, Insook Kim, Marilyn A. Huestis, and Elliot A. Stein
(2007), "Nicotine Enhances Visuospatial Attention by Deactivating Areas of the Resting
Brain Default Network," J. Neurosci., 27 (13), 3477-89.
Inzlicht, Michael and Jennifer N. Gutsell (2007), "Running on Empty: Neural Signals for SelfControl Failure," Psychological Science, 18 (11), 933-37.
Johnsen, Bjorn Helge, Julian F. Thayer, Jon C. Laberg, and Arve E. Asbjornsen (1997),
"Attentional bias in active smokers, abstinent smokers, and nonsmokers," Addictive
Behaviors, 22 (6), 813-17.
Kerns, John C., Jonathan D. Cohen, Angus W. MacDonald Iii, Raymond Y. Cho, V. Andrew
Stenger, and Cameron S. Carter (2004), "Anterior Cingulate Conflict Monitoring and
Adjustments inControl," Science, 303 (5660), 1023-26.
Knoch, Daria and Ernst Fehr (2007), "The Right Prefrontal Cortex and Self-Control," Annals of the
New York Academy of Sciences, 1104 (1), 123-34.
Lancaster, J.L., M.G. Woldorff, L.M. Parsons, M. Liotti, C.S. Freitas, L. Rainey, P.V. Kochunov,
D. Nickerson, S.A. Mikiten, and P.T. Fox (2000), "Automated Talairach Atlas Labels for
Functional Brain Mapping," Human Brain Mapping, 10, 120-31.
Lancaster, Jack and Peter Fox (2008), "Talairach Daemon." San Antonio, TX.
5
Lane, Richard D., Eric M. Reiman, Beatrice Axelrod, Lang-Sheng Yun, Andrew Holmes, and Gary
E. Schwartz (1998), "Neural Correlates of Levels of Emotional Awareness: Evidence of an
Interaction between Emotion and Attention in the Anterior Cingulate Cortex," Journal of
Cognitive Neuroscience, 10 (4), 525-35.
Li, Chiang-shan Ray and Rajita Sinha (2008), "Inhibitory control and emotional stress regulation:
Neuroimaging evidence for frontal-limbic dysfunction in psycho-stimulant addiction,"
Neuroscience & Biobehavioral Reviews, 32 (3), 581-97.
Liddle, Peter F., Kent A. Kiehl, and Andra M. Smith (2001), "Event-related fMRI study of response
inhibition," Human Brain Mapping, 12 (2), 100-09.
Mazoyer, B., L. Zago, E. Mellet, S. Bricogne, O. Etard, O. Houdé, F. Crivello, M. Joliot, L. Petit,
and N. Tzourio-Mazoyer (2001), "Cortical networks for working memory and executive
functions sustain the conscious resting state in man," Brain Research Bulletin, 54 (3), 28798.
McKiernan, Kristen A., Jacqueline N. Kaufman, Jane Kucera-Thompson, and Jeffrey R. Binder
(2003), "A Parametric Manipulation of Factors Affecting Task-induced Deactivation in
Functional Neuroimaging," Journal of Cognitive Neuroscience, 15 (3), 394-408.
Meyer, Roger E. (1988), "Conditioning Phenomena and the Problem of Relapse in Opioid Addicts
and Alcoholics," in Learning Factors in Substance Abuse, Barbara A. Ray (Ed.).
Washington, DC: NIDA.
Mogg, Karin and Brendan P. Bradley (2002), "Selective processing of smoking-related cues in
smokers: manipulation of deprivation level and comparison of three measures of processing
bias," Journal of Psychopharmacology, 16 (4), 385-92.
Munafo, Marcus, Karin Mogg, Sarah Roberts, Brendan P. Bradley, and Michael Murphy (2003),
"Selective Processing of Smoking-Related Cues in Current Smokers, Ex-Smokers and
Never-Smokers on the Modified Stroop Task," J Psychopharmacol, 17 (3), 310-16.
Park, Mi-Sook, Jin-Hun Sohn, Ji- A. Suk, Sook-Hee Kim, Sunju Sohn, and Richard Sparacio
(2007), "Brain substrates of craving to alcohol cues in subjects with alcohol use disorder,"
Alcohol Alcohol., 42 (5), 417-22.
Payne, Thomas J., Patrick O. Smith, Lois V. Sturges, and Sharon A. Holleran (1996), "Reactivity to
smoking cues: Mediating roles of nicotine dependence and duration of deprivation,"
Addictive Behaviors, 21 (2), 139-54.
Pierce, John P., David M. Burns, Elizabeth Whalen, Bradley Rosbrook, Donald Shopland, and
Michael Johnson (1991), "Does Tobacco Advertising Target Young People to Start
Smoking? Evidence from California," Journal of the American Medical Association, 272
(8), 608-11.
Pollay, Richard W (2005), "The Richard Pollay Tobacco Advertising Collection at Roswell Park
Cancer Institute."
6
Pollay, Richard W. (1986), "The distorted mirror: Reflections on the unintended consequences of
advertising," Journal of Marketing, 50 (2), 18-36.
Pollay, Richard W., S. Siddarth, Michael Siegel, Anne Haddix, Robert K. Merritt, Gary A. Giovino,
and Michael P. Eriksen (1996a), "The last straw? Cigarette advertising and realized market
shares among youths and adults," Journal of Marketing, 60 (2), 1.
Pollay, Richard W., S. Siddarth, Michael Siegel, Anne Haddix, Robert K. Merritt, Gary Giovino,
and Michael P. Eriksen (1996b), "The Last Straw? Cigarette Advertising and Realized
Market Share Amoung Youths and Adults, 1979-1993," Journal of Marketing, 60 (2), 1.
Potenza, Marc N., Marvin A. Steinberg, Pawel Skudlarski, Robert K. Fulbright, Cheryl M. Lacadie,
Mary K. Wilber, Bruce J. Rounsaville, John C. Gore, and Bruce E. Wexler (2003),
"Gambling Urges in Pathological Gambling: A Functional Magnetic Resonance Imaging
Study," Archives of General Psychiatry, 60 (8), 828-36.
Raichle, Marcus E., Ann Mary MacLeod, Abraham Z. Snyder, William J. Powers, Debra A.
Gusnard, and Gordon L. Shulman (2001), "A default mode of brain function," Proceedings
of the National Academy of Sciences of the United States of America, 98 (2), 676-82.
Richeson, Jennifer A., Abigail A. Baird, Heather L. Gordon, Todd F. Heatherton, Carrie L. Wyland,
Sophie Trawalter, and J. Nicole Shelton (2003), "An fMRI investigation of the impact of
interracial contact on executive function," Nature Neuroscience, 6 (12), 1323-28.
Robinson, Terry E. and Kent C. Berridge (2003), "Addiction," Annual Review of Psychology, 54,
25-53.
---- (2001), "Incentive-sensitization and addiction," Addiction, 96, 103-14.
---- (1993), "The neural basis of drug craving: an incentive-sensitization theory of addiction," Brain
Research Reviews, 18 (1993), 247-91.
Sayette, Michael A. and Michael R. Hufford (1994), "Effects of Cue Exposure and Deprivation on
Cognitive Resources in Smokers," Journal of Abnormal Psychology, 103 (4), 812-15.
Shulman, Gordon L., Julie A. Fiez, Maurizio Corbetta, Randy L. Buckner, Francis M. Miezin,
Marcus E. Raichle, and Steven E. Petersen (1997), "Common Blood Flow Changes across
Visual Tasks: 11. Decreases in Cerebral Cortex," Journal of Cognitive Neuroscience.
Sinha, Rajita, Cheryl Lacadie, Pawel Skudlarski, and Bruce E. Wexler (2004), "Neural Circuits
Underlying Emotional Distress in Humans," Annals of the New York Academy of Sciences,
1032 (Biobehavioral Stress Response: Protective and Damaging Effects), 254-57.
Stippekohl, Bastian, Markus Winkler, Ronald F. Mucha, Paul Pauli, Bertram Walter, Dieter Vaitl,
and Rudolf Stark (2010), "Neural Responses to BEGIN- and END-Stimuli of the Smoking
Ritual in Nonsmokers, Nondeprived Smokers, and Deprived Smokers,"
Neuropsychopharmacology.
7
Stritzke, Werner G.K., Mary Jo Breiner, John J. Curtin, and Alan R. Lang (2004), "Assessment of
Substance Cue Reactivity: Advances in Reliability, Specificity, and Validity," Psychology of
Addictive Behaviors, 18 (2), 148-59.
Tapert, Susan F., Gregory G. Brown, Sandra S. Kindermann, Erick H. Cheung, Lawrence R. Frank,
and Sandra A. Brown (2001), "fMRI measurement of brain dysfunction in alcoholdependent young women," Alcoholism: Clinical & Experimental Research, 25 (2), 236-45.
Tapert, Susan F., Erick H. Cheung, Gregory G. Brown, Frank R. Lawrence, Martin P. Paulus,
Alecia D. Schweinsburg, M J Meloy, and Sandra A Brown (2003), "Neural response to
alcohol stimuli in adolescents with alcohol use disorder," Archives of General Psychiatry, 60
(7), 727-35.
The FIL Methods Group (2006), "SPM5 Manual." London, UK: Functional Imaging Laboratory,
Wellcome Department of Imaging Neuroscience.
Turkkan, Jaylan S., Mary E. McCaul, and Maxine L. Stitzer (1989), "Psychophysiological Effects
of Alcohol-related Stimuli: II. Enhancement with Alcohol Availability," Alcoholism:
Clinical and Experimental Research, 13 (3), 392-98.
van Veen, Vincent and Cameron S. Carter (2002), "The anterior cingulate as a conflict monitor:
fMRI and ERP studies," Physiology & Behavior, 77 (4-5), 477-82.
Volkow, Nora D. and Joanna S. Fowler (2000), "Addiction, a Disease of Compulsion and Drive:
Involvement of the Orbitofrontal Cortex," Cereb. Cortex, 10 (3), 318-25.
Volkow, Nora D., Joanna S. Fowler, Gene-Jack Wang, Frank Telang, Jean Logan, Millard Jayne,
Yeming Ma, Kith Pradhan, Christopher Wong, and James M. Swanson (2010), "Cognitive
control of drug craving inhibits brain reward regions in cocaine abusers," NeuroImage, 49
(3), 2536-43.
Yang, Zheng, Jun Xie, Yong-Cong Shao, Chun-Ming Xie, Li-Ping Fu, De-Jun Li, Ming Fan, Lin
Ma, and Shi-Jiang Li (2008), "Dynamic neural responses to cue-reactivity paradigms in
heroin-dependent users: An fMRI study," Human Brain Mapping, 9999 (9999), NA.
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