Smoke signals: A study of the neurophysiological reaction of smokers and non-smokers to smoking cues inserted into antismoking public service announcements
Introduction
Tobacco smoke is the second leading cause of death in the world and the first reason of preventable death killing eight million people each year, through heart disease, lung cancer and other illnesses, plus passive smoking (WHO report, 20192).
Numerous public measures have been set up to fight this problem (National Cancer Institute, 20183) and Public Service Announcements (PSAs) represent one of the most effective strategies to influence citizen behavioral changes (Hornik, 2002; Davis et al., 2008; Lee et al., 2011).
DSM 5th edition includes tobacco addiction in “Substance-related disorders” category, recognizing nicotine's ability to develop addiction in humans (American Psychiatric Association, 2013; Benowitz, 2010). Scientific evidence shows that nicotine acts on the meso-limbic dopamine system (Nestler, 2001, Nestler, 2005; Wise, 2004; Koob and Le Moal, 2001; Koob and Wolkow, 2010; Hyman et al., 2006), that projects from the Ventral Tegmental Area (VTA) to the Nucleus Accubens (NAc) and has been implicated in the rewarding effects of drugs abuse (Wise and Bozarth, 1987; Koob, 1992; Wise, 1996; McBride et al., 1999; Pierce and Kumaresan, 2006).
Nicotinic receptors in the meso-limbic system therefore constitutes the fundamental neurobiological substratum in the mediation of the gratifying effects of nicotine and of the development of tobacco addiction (Pidoplichko et al., 2004; Balfour, 2004).
Neuroimaging investigations provide tangible confirmations of how smoking induces dopamine release in the NAc (Brody et al., 2002; Sharma and Brody, 2009) and so how nicotine allows the establishment of pathological dependency behaviors (Carter and Tiffany, 1999). However, numerous factors including genetic baggage (Agrawall et al., 2012; Bierut et al., 2007), gene-environment interactions in development (Tully et al., 2010; Kendler et al., 2008) personality traits (Terraciano and Costa, 2004; Zuckermann et al., 1990), metacognitions about smoking (Nikčević and Spada, 2010) psychosocial factors (Chassin et al., 2000; White et al., 2002), age (DeBry and Tiffany, 2008) and mental illness (Prochaska et al., 2017) contribute or co-occur with addiction.
Nicotine is essential in addiction development, but only after extensive self-administration experience, while nicotine-associated cues can powerfully affect self-administration behaviors. Thus, although the dependent smoker may smoke to quell or achieve internal states (e.g., to reduce negative moods), external cues can powerfully influence self-administration behaviors (Baker et al., 2004). In fact, non-nicotinic factors play a fundamental role in addiction (Caggiula et al., 2001) as confirmed by the non-univocal results found in the therapeutic strategies directed to the action of nicotine - Nicotine Replacement Therapy (NRT) (Silagy et al., 2004).
Indeed a smoker is not a mere nicotine's self-administrator: many stimuli are associated with smoking behavior (Benowitz, 2009). Smoking desire is triggered by stimuli associated to nicotine's intake, such as people, environments and mood status (Tiffany & Tiffany and Drobes, 1990; Michalowski and Erblich, 2014; Conklin et al., 2015). So, a “Smoking Cue (SC)” is defined as a visual cue eliciting smoking urges in adult smokers and that represents at least one of the following: (a) smoking-related materials (i.e., cigarettes, ashtrays), (b) holding and handling of a cigarette without smoking it, and (c) actual smoking of a cigarette (Kang et al., 2009; Hutchinson et al., 1999; Tiffany et al., 2000; Waters et al., 2004).
SCs' role in relapse contrast in smokers wishing to quit is well known (Ikard et al., 1969; Droungas et al., 1995; Shiffman et al., 2013; Shiffman, 1982). The development of automatic associative processes with repeated tobacco-use could be as powerful as the direct effects of smoking (Brunzell and Picciotto, 2009). The basis of nicotine addiction is a combination of positive reinforcements, including enhancement of mood and avoidance of withdrawal symptoms, and conditioning has a crucial role in the development of tobacco addiction (Benowitz, 2009).
Classical pavlovian conditioning paradigm (Pavlov, 1927) offers the theoretical framework for understanding the learning processes developed in nicotine addiction (Bevins and Palmatier, 2004; Bevins and Murray, 2011; USDHHS Report, 2010).
Conditioned stimuli (CSs) to cigarettes smoke act as motivational magnets following repeated association with unconditioned stimuli (UCSs) (Berridge et al., 2009).
According to Robinson and Berridge's “Incentive Sensitization Theory” (IST), repeated exposure to potentially addictive substances such as nicotine can induce brain changes to circuits that mediate the psychological processes involved in motivated behavior: the attribution of incentive salience to CS (Robinson and Berridge, 2008). Addicted behaviors are due to progressive and persistent neuroadaptations caused by the repeated use of substances: changes in nervous system manifest both neurochemically and behaviorally through the phenomenon of “sensitization”, defined as hypersensitivity to incentive motivational effects of drugs and their associated stimuli (Robinson and Berridge, 2003).
Over time, the mesolimbic dopamine system's sensitization transforms drug-related cues in motivational magnets (Berridge et al., 2009; Robinson and Berridge, 2013). Repeated pavlovian CS-UCS association increases the predictive value of the CS relative to the UCS, a process that can be described in terms of correlation and computational models (Anselme et al., 2013).
This theoretical framework could explain how smokers, despite the awareness of nicotine's danger, continue smoking compulsively often not feeling any pleasure and failing to explain the motivations of their behavior (Baker et al., 2004). Moreover, since the neuroadaptation induced by the substance is often permanent, it is hypothesized that is precisely the presence of the sensitization connected to these brain modifications of reward's circuit that makes smokers particularly sensitive to drug-related cues, causing relapse with evident clinical implications (Robinson and Berridge, 2000).
IST's pillars are reflected in experimental neurophysiological designs based on the reactivity of smokers to SCs. Winkler et al. (2011) clearly support how a neutral stimulus can elicit preparatory physiological responses if associated with smoking. Carter and Tiffany (1999) support the value of the experimental paradigm of cue reactivity by emphasizing how it induces physiological responses and craving in smokers and is therefore a valuable tool for investigating smoke addiction. Further confirmations are obtained from studies carried out through electroencephalography (EEG). Zinser et al. (1999) observe in smokers, a greater activation of the left hemisphere to the vision of SCs: results would therefore be congruent with the IST, representing the demonstration that approach motivation connected to the increased activation of the left frontal cortex (Davidson, 2004) is sensitive to stimuli associated with the rewarding substance. Studies in humans, show how levels of nicotine addiction influence electrophysiological activity (Haarer and Polich, 2000) and fMRI studies highlight how tobacco advertisement elicits cigarette craving and different neuronal activity in response to SCs primarily in smokers, indicating that they might be particularly responsive towards external SCs (Vollstädt-Klein et al., 2011). Moreover, literature illustrates how nicotine administration increases EEG activity shifting from low-frequency to high-frequencies activity (Teneggi et al., 2004; Knott, 2001; Domino, 2003) and how smoking deprivation is associated with shifts regarding the balance of Alpha activity between the left versus the right frontal hemisphere (Zinser et al., 1999).
The aim of the study is to assess, through EEG patterns, the possible ineffectiveness of media intervention, (for a comparative analysis of antismoking PSA see Wakefield et al., 2003) depending on target population's smoking habit.
In accord to Incentive Sensitization Theory basis here it is therefore hypothesized that heavy smokers would present a significantly different electrophysiological profile in comparison to light and non-smokers during antismoking PSA's vision depending on the appearance of SCs, and hence of the possible “boomerang effect” produced by them (Harris et al., 2014).
It is important to state that to our best knowledge, any previous EEG study investigated the reactivity to SCs in antismoking PSAs in the light of the IST.
Section snippets
Participants
92 adult volunteers were recruited (46 M, 46F; average age = 34.70 ± 0.08 years old) subdivided in 31 Heavy Smokers (HS - 16 M, 15F), 31 Light Smokers (LS - 13 M, 18F) and 30 Non-Smokers (NS - 17 M, 13F). Participants smoking >5 cigarettes per day were classified as HS (Shiffman and Paty, 2006; Shiffman, 2009; Schane et al., 2010; Husten, 2009; Bjartveit and Tverdal, 2005); participants who did not smoke any cigarette were classified as NS. Subjects received detailed information on the study
Approach withdrawal index (AW)
AW Index related to “The Breath Holder” stimulus highlighted a statistically significant interaction Smoking Cue × Gender F (1,83) = 5689, p =,019 and Cue × Smoking Habit × Gender, F (2,85) = 4121, p =,019. In particular, post hoc analysis revealed significant differences in the AW values: HS Females showed higher AW values both with respect to the NS Females (p =,029) and to HS Males (p =,027). Moreover, HS Females showed higher AW levels in the Post-Cue in comparison to the Pre-Cue segment (p
Discussion
In this study, HS, LS and NS groups' frontal EEG Alpha and Theta oscillations were analyzed in response to SC presented in antismoking PSAs and it has been found a major activation in both bands in the Post-Cue phase in the HS female group. This finding could help to understand the ‘boomerang effect’ elicited by some antismoking PSAs (Harris et al., 2014) in the smoking habit because of the presence of SC.
It is known that exposure to cigarette-related cues is thought to precipitate smoking
Conclusions
Results show that SC presence in antismoking PSAs have reliable effects on EEG frontal activation. Specifically, AW Index data confirm the initial hypothesis: according to IST, SCs inserted in PSAs built on a communicative style based on happiness, can elicit in HS (especially if females) different neurophysiological responses compared to a NS population. In particular, this could be interpreted as an activation signal related to smoking, possibly contributing to the maintenance of the
Grant funding sources
The present work was funded by the European Commission by Horizon 2020 project HCO-06-2015, “SmokeFreeBrain” grant no. 681120.
Authors' contributions
BMSI and GC wrote the manuscript; BMSI, GC and EM performed the statistical analysis; BMSI and EM performed the data analysis; BMSI, GC, EM, DR and ACML performed the data recording; PC, LT, ACML and FB edited the manuscript; FB, supervised the project.
Declaration of competing interest
The authors declare no conflict of interest.
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These authors have contributed equally to this work.