RESEARCH REPORT doi:10.1111/j.1360-0443.2009.02760.x

The impact of cigarette deprivation and cigarette

availability on cue–reactivity in smokersadd_2760 364..372

Steffani R. Bailey1, Katherine C. Goedeker2 & Stephen T. Tiffany3 Stanford University School of Medicine, Stanford Prevention Research Center, Palo Alto, CA, USA,1 Purdue University,West Lafayette, IN, USA2 and University at Buffalo,The State University of New York, Buffalo, NY, USA3

ABSTRACT

Aims This experiment was conducted to determine the impact of cigarette deprivation and cigarette availability on reactivity measures to cigarette cues. Participants Smokers were recruited who were 18 years of age or older, not attempting to quit or cut down on their , smoked at least 20 cigarettes daily, had been smoking regularly for past year and had an expired carbon monoxide level of at least 10 parts per million. Design Smokers were assigned randomly to abstain from smoking for 24 hours (n = 51) or continue smoking their regular amount (n = 50). Twenty- four hours later, they were exposed to trials of either a lit cigarette or a glass of water with a 0, 50 or 100% probability of being able to sample the cue on each trial. Craving, mood, heart rate, skin conductance, puff topography and latency to access door to sample the cue were measured. Findings Both exposure to cigarette cues and increasing availability of those cues produced higher levels of craving to smoke. Deprivation produced a generalized increase in craving. There was no consistent evidence, however, that even under conditions of high cigarette availability, deprived smokers were sensitized selectively to presentations of cigarette cues. Conclusions The data suggest that, even under conditions of immediate cigarette availability, deprivation and cue presentations have independent, additive effects on self-reported craving levels in smokers.

Keywords Cigarette availability, cigarette deprivation, craving, cue–reactivity.

Correspondence to: Stephen T. Tiffany, University at Buffalo, SUNY, Department of Psychology 228 Park Hall, Buffalo, NY 14260-4110, USA. E-mail: [email protected] Submitted 4 March 2009; initial review completed 16 April 2009; final version accepted 28 July 2009

INTRODUCTION account for smokers’ beliefs that they will confront intense craving when they are deprived of cigarettes [13]. Craving is a core feature of tobacco [1,2]. The proposal that abstinence should amplify cue-specific Although there is continuing controversy about the craving has considerable theoretical support. In their nature and functional significance of craving, laboratory- incentive motivational theory of drug addiction, Stewart based studies have isolated several factors that modulate and colleagues [14] hypothesized that drug deprivation craving processes reliably.In the case of cigarette smokers, should increase the salience of drug cues and decrease smokingdeprivation(e.g.[3,4]),smoking-relatedcues[5], the threshold for craving activation. Similarly, Baker and stressors [6,7], induction of negative affect (e.g. [8,9]) colleagues [15] invoked incentive motivational processes and alcohol intoxication (e.g. [10–12]) readily increase in predicting that drug deprivation should sensitize the craving to smoke. Less clear is the extent to which these craving responses of drug users to drug-related cues. conditions might interact to control craving processes. These propositions are consistent with general incentive Certain combinations of evocative stimuli could motivational models that presume that the salience of operate synergistically to produce especially intense levels motivationally relevant cues is modified selectively by the of craving. In particular, nicotine deprivation might deprivation state of the organism (e.g. [16–18]). prime smokers’ reactions to smoking-related cues so that Although plausible, the assumption that cigarette they would be hyper-reactive to those cues when absti- abstinence amplifies smokers’ cue-specific craving has nent from cigarettes. Indeed, such an effect might little empirical support. Maude-Griffin & Tiffany [9] found

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 The impact of cigarette deprivation 365 that smokers abstinent for 6 or 24 hours reported gener- conductance and shorter latency to access the cigarette in alized elevations in craving relative to non-abstaining comparison to neutral trials [37]. If cigarette availability smokers. However, they obtained no evidence of any moderates the impact of abstinence on smokers’ craving selective increase in deprived smokers’ craving, mood or reactions to smoking cues, then nicotine-deprived physiological reactions to smoking-related cues. A similar smokers who are exposed to a cigarette they believe they pattern has been reported by numerous other researchers can smoke immediately should display disproportionately [19–26]. Abstinence-induced craving appears to be con- stronger craving reactions to that cue relative to non- trolled by nicotine deprivation, as this effect is reversed by deprived smokers under the same availability conditions. nicotine delivered via a nicotine patch [27,28]; however, In contrast, the manipulation of cigarette availability may nicotine patches have no impact on cue-specific craving have no impact on cue-specific craving during cigarette [28–30]. deprivation suggesting that, even under conditions of Although there is little indication of synergistic inter- immediate availability, nicotine-deprived smokers are not actions between nicotine abstinence and cue-specific hyper-reactive to smoking-related cues. craving, that conclusion has to be qualified by the fact that smokers in these studies had no access to cigarettes METHOD when presented with smoking-related cues. Many researchers have posited that expectations of drug avail- Participants ability may regulate addicts’ craving responses to drug A total of 119 (mean = 60, F = 59) smokers were stimuli [15,31–36]. The opportunity to smoke a cigarette recruited from the local community using flyers and immediately after the presentation of a smoking cue can newspaper advertisements. Eligible participants were increase the level of craving markedly to the cue presen- aged 18 years or older, not attempting to quit or cut down tation (e.g. [37,38]). The unavailability of cigarettes on their smoking, smoked at least 20 cigarettes daily, had might moderate the impact of abstinence on craving been smoking regularly for the past year and had an reactivity to smoking cues. Given that immediate ciga- expired carbon monoxide (CO) level of at least 10 parts rette availability can amplify craving to smoking-related per million (p.p.m.). cues, cigarette unavailability may suppress any height- ened cue–reactivity that deprived smokers might display Procedures normally if given the opportunity to smoke. This hypothesis was evaluated partially by McBride Session 1 and colleagues [22], who examined the joint impact of Participants signed a consent document and CO levels cigarette abstinence and smoking availability on cue- were assessed with a Vitolograph CO monitor. Partici- induced cigarette craving. In that study, availability was pants completed the Mood Form [39] and the Question- manipulated by telling participants that they could or naire on Smoking Urges (QSU; [4]). Participants then could not smoke after the cue session was completed. smoked one cigarette through the mouthpiece of the Both abstinence and expectancy of post-session smoking CReSS (Clinical Research Support System; Plowshare elevated craving to smoke significantly, but these factors Technology, Richmond, VA, USA) while completing a did not interact. The conclusions from this study were Smoking History Form. Participants were then assigned limited by the absence of direct evidence that the avail- randomly to either the deprived or non-deprived groups. ability manipulation enhanced cue-specific craving. This Those in the deprived group were instructed to remain is not surprising, as cigarette availability is likely to have abstinent from cigarettes or any form of nicotine for the the greatest impact when smokers can smoke immedi- next 24 hours. They were told that smoking would be ately in the presence of the cue [37]. Indeed, research by detectable by the CO analysis at the next session. Partici- Sayette et al. [38] suggests that the cue-specific availabil- pants in the non-deprived group were instructed to smoke ity effect dissipates if smokers have to wait more than 15 at their usual rate between sessions. At the end of session seconds to smoke after presentation of smoking stimuli. 1 participants selected a slip of paper from a box, assign- The present study evaluated the impact of cigarette ing them to either the deprived or smoking condition. All deprivation and immediate cigarette availability on reac- participants received $60 for being in the study.Those in tivity measures using the cue–availability paradigm (CAP; the deprived group received a $30.00 bonus if they [37]). The CAP examines the effects of cigarette availabil- remained completely abstinent between sessions. ity by manipulating the smoker’s immediate access to cigarettes throughout the cue–reactivity session. Session 2 Research with the CAP has shown that increased cigarette availability increased cue–reactivity as indexed by stron- At the beginning of this 90-minute session, CO levels ger craving report, enhanced positive mood, higher skin were determined and participants completed the QSU,

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 366 Steffani R. Bailey et al.

Mood Form and Withdrawal Symptoms Checklist (WSC; On trials that the door was locked, participants were [40]). Participants in the non-deprived group then instructed to close their eyes after attempting to open the smoked a cigarette. Participants in the deprived group door. The interval between trials averaged 30 seconds. were asked to report any form of tobacco use over the Across all participants, the average CAP session duration inter-session interval. The CO criterion for deprivation was 61 minutes (range 53–78 minutes) with an average was a minimum 60% reduction in CO levels from session inter-puff interval of approximately 5 minutes. All par- 1. If a participant did not meet the CO criterion at session ticipants sampled the cigarette on all available trials. 2, the slip of paper for group assignment was returned to the box until we were able to reach our target enrollment. Data reduction and analyses Heart rate and skin conductance were collected as All CAP data were analyzed with a 2 ¥ 2 ¥ 3 ¥ 4 described by Carter & Tiffany [37]. Participants were (group ¥ cue type ¥ probability ¥ block) mixed-design seated in front of a computer monitor and keyboard and analysis of variance. The Greenhouse–Geisser technique wore headphones. A stimulus box, with a clear glass was employed to control for heterogeneity of covariance sliding door on the front, was set into the wall over the across repeated measures. Previous research with the table. A flip-down board on a hinge with a holder for the CAP indicated that the most pronounced physiological CReSS mouthpiece was inside the box. The hinged appa- effects occurred during the 4 seconds just prior to ratus allowed for either a lit cigarette to be placed in the attempting to open the door. Therefore, analyses of the mouthpiece or for a plastic cup of water to be placed on a physiological measures focused on this period. Correla- flat surface of the box. A new cigarette was used for each tional analyses were conducted to determine the extent to cigarette trial and the water cup was refilled on each which relationships between craving and mood and water trial. craving and latency measures reported by Carter & The CAP session consisted of 48 trials (24 cigarette, Tiffany [37] were replicated in the present study. 24 water) with a 0, 50 or 100% probability of being able to open the door on each trial. Cue and probability levels were pseudo-randomized across four blocks of 12 trials RESULTS each (see [37] for randomization procedures). At the beginning of the session, participants closed their eyes Participants and waited for a tone to be presented over the head- The average participant was 30 years old (range 18–61), phones. At the tone, participants opened their eyes and smoked 25 cigarettes daily [standard deviation were given the following information on the monitor: (SD) = 9.12] and smoked his/her first cigarette at 13.7 ‘You have a (0%, 50%, 100%) chance of opening the years of age (range 5–23). There were 50 participants in door. Look in the box and think carefully about what you the non-deprived group (males = 25, females = 25) and see’. A light display below the glass door also indicated 51 participants (males = 25, females = 26) assigned to the probability in effect for that trial. After 8 seconds a the deprived group who met the CO criterion. The average tone was delivered, and participants rated cigarette CO level was 31 p.p.m. (SD = 16.34); deprived = craving and mood items presented on the monitor by 28 p.p.m., non-deprived = 35 p.p.m.; not significant (NS) entering a number on a 1–7 scale via the keyboard. Ciga- at session 1, and 4.2 (SD = 3.63) and 33.7 p.p.m. rette craving was measured by a four-item subscale of the (SD = 16.76) for the deprived and non-deprived groups, QSU ([4]; see [37] for item wording). All items were pre- respectively, at session 2. On average, smokers in the sented in a randomized order with the craving questions deprived condition had an 84% decrease in their CO levels always presented first. from session 1 to session 2. Participants in the non- After the final item was rated, participants waited for 8 deprived group reported smoking their last cigarette an seconds. This period was terminated by a tone and average of 23.4 minutes (range of 5–600 minutes; instructions to attempt to open the door and sample the median = 10 minutes) prior to the start of session 2. An cue (either a sip of water or one puff of the cigarette as additional 18 individuals (10 males, eight females) explained by a research assistant prior to the CAP assigned to the deprived group were excluded from analy- session). The CReSS recorded puff topography on the ciga- ses as they did not meet the abstinence criteria. These rette trials. Participants were told that they should individuals did not differ significantly from those who met attempt to open the door on 0% probability trials to the abstinence criteria on any session 1 measures. equate the level of physical movement across every trial. Latency (in msec) was recorded on every trial through a Questionnaires micro-switch located in the door of the stimulus box. Par- ticipants were then instructed to close the door, close There were no significant differences between groups at their eyes and wait for the tone signaling the next trial. session 1 on the QSU or Mood Form. At the beginning of

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 The impact of cigarette deprivation 367

Table 1 Means and standard deviations (in parentheses) for 4.8 Deprived Cigarette negative and positive mood ratings at the 0%, 50% and 100% cigarette and water trials. 4.4 Water Probability

Cigarette 0% 50% 100% 4 Non-Deprived

Negative mood rating Craving Stimulus 3.6 Water Cigarette 3.34 (1.68) 3.09 (1.53) 2.60 (1.39) Water 3.13 (1.57) 3.02 (1.56) 3.08 (1.61) Positive mood rating 3.2 Stimulus 1 Cigarette 3.98 (1.62) 4.45 (1.48) .92 (1.49) 0% 50% 100% Water 4.23 (1.59) 4.27 (1.58) 4.23 (1.67) Probability For each rating type, statistically significant cigarette/water differences at Figure 1 Average self-reported craving (scale of 1–7) for deprived each probability level are shown in bold type. and non-deprived conditions by stimulus type and probability

the door would be unlocked on cigarette trials (Table 1). session 2, relative to the non-deprived group, smokers There were significant interactions between cue type and in the deprived group reported significantly stronger probability for both positive and negative mood ratings, craving to smoke on the general factor scale and both Fs Ն 23.13, Ps < 0.0001, where cigarette trials pro- subscales of the QSU, Fs Ն 15.32, Ps < 0.001, sig- (2, 198) (1, 99) duced significantly higher negative mood ratings and nificantly stronger negative mood on the Mood Form lower positive mood ratings than water trials on the 0% F = 6.40, P < 0.05 and significantly higher scores on (1, 99) probability level. This pattern was reversed on the 100% the craving, psychological discomfort and physical symp- probability level, with negative mood ratings significantly toms scales of the WSC, Fs Ն 6.56, Ps < 0.05. (1, 99) lower and positive mood ratings significantly higher on cigarette trials compared to water trials. CAP trials

Craving Puff topography

During CAP trials (Fig. 1), participants in the deprived Due to equipment malfunction, complete CReSS data group reported significantly higher craving for cigarettes were not available from 15 participants (seven in the than those in the non-deprived group, F(1, 99) = 7.41, deprived group and eight in the non-deprived group). P < 0.01. Participants also reported significantly stronger Among those participants with complete CReSS data, craving on cigarette trials compared to water trials, there were no significant main effects or interactions

F(1, 99) = 107.44, P < 0.0001. Craving became signifi- on either puff duration or maximum flow. Puff volume cantly stronger as the probability increased that the was significantly higher for the non-deprived group participant could open the door and sample the cue, (mean = 64.64 ml, SD = 17.83) than for the deprived

F(2, 198) = 39.74, P < 0.0001; however, an evaluation of a group (mean = 58.90 ml, SD = 20.66), F(1, 84) = 4.12, significant cue–probability interaction, F(2, 198) = 10.05, P < 0.05. Participants also had significantly greater P < 0.0001, revealed that the increase in craving by puff volume on the 100% trials (mean = 62.70 ml, probability level was significant only in cigarette trials. SD = 19.31) relative to 50% trials (mean = 60.84 ml,

There were no significant interactions between the absti- SD = 19.18), F(1, 84) = 4.34, P < 0.05. nence manipulation and either cue or probability factors and no significant effects involving the block factor. Latency

The deprived group had significantly shorter latencies Mood to access the door than the non-deprived group,

The deprivation manipulation (deprived versus non- F(1, 98) = 4.45, P < 0.05. There was also a significant prob- deprived) produced no significant main effects or inter- ability effect, F(2, 196) = 26.12, P < 0.0001, a block effect, actions on mood ratings collected during CAP. The F(3, 294) = 9.17, P < 0.0001, a cue–probability interac- manipulation of cues and probability produced comple- tion, F(2, 196) = 3.24, P < 0.05 and a group–probability mentaryeffectsonmoodratings;negativemooddecreased interaction, F(2, 196) = 4.15, P < 0.05. Latency on both and positive mood increased with greater probability that cigarette and water trials were shorter, with increasing

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 368 Steffani R. Bailey et al.

Table 2 Means and standard deviations (in parentheses) for latency to open the door (in msecs) at the 0%, 50% and 100% cigarette and water trials for each group condition.

Probability

0% 50% 100%

Non-deprived group Stimulus Cigarette 2298.7 (431.7) 2228.3 (545.9) 2123.7 (552.7) Water 2240.7 (370.4) 2209.1 (414.5) 2157.0 (437.5) Deprived group Stimulus Cigarette 2224.9 (436.6) 1967.8 (401.1) 1920.5 (464.5) Water 2171.1 (410.1) 2062.9 (401.9) 1947.3 (401.6)

probability of being able to open the door for both 0.35 groups (see Table 2). In general, door-opening latencies Cigarette decreased across trial blocks. Plotting the cue–probability 0.3 Deprived Non-Deprived interaction revealed a cross-over effect such that, unlike at the 50% and 100% probability levels where cigarette 0.25 trials had shorter latencies than water trials, the opposite was true at the 0% probability trials. Analysis of the 0.2 group–probability interaction revealed a significant 0.15 difference between the deprived and the non-deprived Cigarette groups at 50% and 100% probability levels with shorter Water latencies for both cue types for the deprived group. 0.1 Water

0.05 Physiological responses Skin Conductance Deviations (u-siemens) Skin Conductance Deviations Skin conductance 0 0% 50% 100% There were no significant baseline differences between Probability the deprived and non-deprived groups. During the 4 seconds just prior to attempting to open the door (see Figure 2 Skin conductance deviations for deprived and non- Fig. 2), the deprived group had significantly higher levels deprived conditions by stimulus type and probability during the 4 of skin conductance than the non-deprived group, seconds prior to attempting to open the door

F(1, 99) = 4.82, P < 0.05. Across both groups, cigarette trials were associated with higher levels of skin conduc- tance than water trials, F(1, 99) = 48.97, P < 0.0001. Heart rate There was also a main effect for probability, There were no significant effects in the analyses of the F = 10.19, P < 0.0001, a significant cue–group (2, 198) heart rate data. interaction, F(1, 99) = 6.65, P < 0.05, cue–probability interaction, F = 4.73, P < 0.05 and a cue– (2, 198) Correlational analysis probability–group interaction, F(2, 198) = 6.57, P < 0.01. Analysis of the cue–probability interaction revealed that Carter & Tiffany [37] found that the strongest associates the difference in skin conductance between cigarette and of craving on trials where the cue–reactivity effects were water trials at the 100% probability level was signifi- the most pronounced (i.e. 100% cigarette trials) were the cantly larger than the difference at both the 0% and 50% negative mood ratings collected from trials where ciga- probability levels. Analysis of the cue–group and the cue– rettes were unavailable (i.e. 0% cigarette trials). In con- probability–group interactions revealed that this differ- trast, the mood ratings (either negative or positive mood) ence between cue trials at the 100% probability level on 100% cigarette trials were not correlated significantly compared to the 0% and 50% probability levels was sig- with craving ratings on those same trials. The mood- nificant for the deprived group only. craving correlations from the present study replicated

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 The impact of cigarette deprivation 369

Table 3 Correlations of craving on 100% probability cigarette colleagues [26] found that overnight cigarette abstinence trials with negative mood and positive mood on cigarette trials reduced cue–reactive craving relative to a non-abstinent (at 0, 50 and 100% probability) for each group condition. condition. In that study, cue–reactivity was indexed as a Group difference from baseline responding, a procedure that may provide a less sensitive assessment than measuring Mood/cigarette Deprived Non-deprived reactivity as response difference between drug cues and probability (n = 51) (n = 50) neutral cues [41]. Indeed, a subsequent study from that same group [20], in which cue–reactivity was indexed as Negative/0% 0.40** 0.43** Negative/50% 0.31* 0.38** craving differences between smoking and neutral cues, Negative/100% 0.04 0.23 found no evidence that abstinence moderated the magni- Positive/0% -0.33* -0.27 tude of cue–reactive craving. Positive/50% -0.07 -0.07 The finding that negative mood was elevated in ciga- Positive/100% 0.14 0.13 rette trials relative to neutral cues parallels mood effects observed in conventional cue–reactivity studies in which *P < 0.05, **P < 0.01. smokers have no immediate access to cigarettes during cue exposures (see [42] for review). The reversal of this this pattern. Negative mood on cigarette trials when there pattern, when cigarettes were immediately accessible, was a 0% or 50% probability of being able to open the replicates previous CAP findings [37]. Thus, the mood door was correlated significantly with craving on 100% ratings were sensitive to both the cue and availability cigarette trials for both groups (see Table 3). For the manipulation but were not affected by cigarette depriva- deprived group only, positive mood on cigarette trials tion. There also was no evidence in the mood ratings of when there was a 0% probability of being able to open the any interactions between deprivation and cue–reactivity door was correlated significantly (negatively) with or between deprivation and cigarette availability. That is, craving on cigarette trials. as with craving, there was no indication in mood report of Every correlation between latency to access the door any abstinence-induced sensitization to smoking cues. on cigarette trials and craving on both the cigarette and The fact that both craving and positive mood water trials was significant for the deprived group. All increased with cigarette availability may suggest that these correlations were negative (rs ranged from -0.282 smokers were expressing pleasure in anticipation of to -0.473; median =-0.382, Ps Յ 0.05), with the stron- smoking [15,43]; however, there was no evidence that gest correlation between craving and latency on the ciga- positive mood was indexing the emotional valence of rette trials with 100% probability to sample the cue. craving as there were no significant positive correlations For the non-deprived group, the only significant correla- between craving report and positive mood. An alternative tion was between craving on 50% probability cigarette hypothesis is that smokers were expressing relief that trials and latency on 100% probability cigarette trials they could smoke on 100% probability cigarette trials and (r =-0.307, P < 0.05). There were no other significant frustration when they knew they could not smoke or were correlations across self-reports, physiological responding uncertain of cigarette availability [37]. The finding that or latency. positive correlations between negative mood and craving were significant at the 0% and 50% probability levels, but DISCUSSION not at the 100% probability level, lends support to this As has been found in previous studies [2,37], 24 hours of interpretation. This pattern of mood results complements cigarette deprivation produced generalized increases in previous findings from other studies that negative mood, craving, and immediate cigarette availability boosted not positive mood, is linked most clearly with craving craving reactivity to smoking-related cues. Deprivation- processes (see [42] for review). enhanced craving was evident in multi-dimensional Although the self-report data did not support the pre- craving and nicotine withdrawal questionnaires admin- dictions derived from several incentive motivational istered just prior to the cue manipulation as well as on models of the impact of deprivation on reactivity to moti- the craving measure given repeatedly during the cue- vationally relevant cues, there was evidence in skin con- availability procedure. Despite the robust main effects for ductance responses of an interaction between abstinence cigarette deprivation and availability, there was no con- and smoking cues. As has been observed in previous sistent evidence that, even under conditions of immediate research (e.g. [19]), skin conductance responses were cigarette availability, deprivation enhanced cue-induced larger in the presence of cigarette cues relative to water craving selectively. cues. In addition, deprived smokers, but not non-deprived In contrast to the common expectation that absti- smokers, showed particularly strong skin conductance nence should sensitize cue–reactive craving, Powell and responses to cigarette cues on 100% availability trials.

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 370 Steffani R. Bailey et al.

The magnitude of the difference in skin conductance sensitive to cue manipulations, and not prone to ceiling responses between the deprived and non-deprived groups effects that might have limited the detection of synergistic on these trials was fairly robust (means of 0.32 and interactions between cue effects and abstinence. These 0.13 m-siemens, respectively), with an estimated effect considerations, in combination with the relatively large size of 0.72 (Cohen’s d). To the best of our knowledge, the sample size used in this research, suggest that the absence finding of increased skin conductance reactivity to of any enhanced reactivity to smoking cues under condi- smoking cues under conditions of cigarette deprivation tions of abstinence was not due to an insensitivity of has not been reported previously in the literature. This craving assessment or lack of experimental power. pattern, if replicated, suggests that skin conductance Some limitations of this study should be noted. Par- may offer unique information about motivational pro- ticipants knew that they could resume smoking immedi- cesses activated by smoking cues in a deprived condition. ately after the session and were deprived of smoking for More generally,these divergent patterns across self-report only 24 hours. Smokers pursuing quitting actively and physiological measures illustrate that cue–reactivity and/or abstinent for a longer duration may show responses are not uniform indices of a homogeneous enhanced sensitivity to cigarette related stimuli. Never- drug-motivational state. Indeed, the absence of signifi- theless, it was clear from the self-report measures that the cant correlations between skin conductance and self- deprived smokers were experiencing symptoms of with- reported craving suggest that these two measures of drawal and stronger craving than those in the non- reactivity may be tracking somewhat independent deprived condition. Another factor that may have affected processes. the results, particularly the lack of significant differences We found that craving to smoke was correlated signifi- in heart rate between groups, is that smokers in the cantly with latency to access the door on both water and deprived group were exposed to 12 puffs of a cigarette cigarette cue trials, but these relationships were restricted during the CAP. Although allowing people to smoke also almost exclusively to smokers in the deprived group. This could have affected craving levels, the amount smoked finding parallels results reported by Sayette and col- was equal to approximately one cigarette, a significantly leagues [44], who found that measures of craving-related lower amount than their typical smoking behavior. Fur- processes were inter-related more strongly when smokers thermore, there were no significant block effects, suggest- were abstinent from cigarettes for 7 hours. A pattern of ing that craving did not change significantly over the enhanced cohesiveness between craving and drug-use course of the session. measures under conditions of cigarette deprivation is Our data are consistent with the hypothesis that dep- consistent with the proposal of Baker et al. [15] that rivation and smoking cue presentations have indepen- correlations between various manifestations of drug- dent, additive effects on craving levels in smokers. Beyond motivational states should increase when drug-use moti- the conceptual implications for models of craving and vation is strongest. In the current study, this pattern was drug-use motivation, these results have important rami- not generalized across all craving correlates. That is, the fications for the assessment and treatment of craving. relationships between mood measures and craving did Several studies of the effects of transdermal nicotine not differ as a function of deprivation. Moreover, the cor- patches on cue-elicited craving in smokers have shown relations between craving and latency measures were not that the nicotine patch had no significant impact on affected markedly by the cue-content of the exposure craving generated by smoking-related cues [28–30]. trials. These results indicate that, similar to the main Such results suggest that treatment may have to selec- effects of deprivation on craving, deprivation promoted tively target craving arising from cue-induced craving greater cohesiveness among craving and certain other and deprivation-induced craving. More generally, the measures, but these correlations were not necessarily present data underscore the value of distinguishing cue-specific. between deprivation-induced and cue-induced craving When examining the impact of abstinence on craving for cigarettes [2]. reactivity,it is useful to employ procedures that maximize the possibility of detecting cue effects across a wide span Acknowledgements of response levels. The CAP allowed for the assessment of This research was funded by an NIH grant R01 DA10264 craving responses across a range of stimulus intensities awarded to S. Tiffany. We thank Virginia A. Edwards and (i.e. availability), aggregated numerous cue trials at each Angela Begle for their help during the data collection level of cue type and availability, assessed craving directly phase of this study. in the presence of the cue, indexed craving reactivity rela- tive to a neutral cue condition and measured craving as Declarations of interest the average of multiple items. Collectively, these features produced a craving assessment that was reliable, highly None.

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 The impact of cigarette deprivation 371

References 20. Dawkins L., Powell J. H., West R., Powell J., Pickering A. A double-blind placebo controlled experimental study of 1. Goedeker K. C., Tiffany S. T. On the nature of nicotine addic- nicotine: I—effects on incentive motivation. Psychopharma- tion: a taxometric analysis. J Abnorm Psychol 2008; 117: cology 2006; 189: 355–67. 896–909. 21. McClernon F. J., Hiott F. B., Huettel S. A., Rose J. E. 2. Tiffany S. T., Warthen M. W., Goedeker K. C. The functional Abstinence-induced changes in self-report craving correlate significance of craving in nicotine dependence. In: Bevans with event-related FMRI responses to smoking cues. Neurop- R. A., Caggiula A. R., editors. The Motivational Impact of sychopharmacology 2005; 30: 1940–7. Nicotine and its Role in Tobacco Use. New York, NY: Springer 22. McBride D., Barrett S. P., Kelly J. T., Aw A., Dagher A. Effects Science; 2009, p. 171–97. of expectancy and abstinence on the neural response to 3. Schuh K. J., Stitzer M. L. Desire to smoke during spaced smoking cues in cigarette smokers: an fMRI study. Neurop- smoking intervals. Psychopharmacology 1995; 120: 289– sychopharmacology 2006; 31: 2728–38. 95. 23. McClernon F. J., Kollins S. H., Lutz A. M., Fitzgerald D. P., 4. Tiffany S. T., Drobes D. J. The development and initial vali- Murray D. W., Redman C. et al. Effects of smoking absti- dation of a questionnaire on smoking urges. Br J Addict nence on adult smokers with and without attention deficit 1991; 86: 1467–76. hyperactivity disorder: results of a preliminary study. Psy- 5. Carter B. L., Tiffany S. T. Meta-analysis of cue–reactivity in chopharmacology 2008; 197: 95–105. addiction research. Addiction 1999; 94: 327–40. 24. McDonough B. E., Warren C. A. Effects of 12-h tobacco 6. Payne T. J., Schare M. L., Levis D. J., Colletti G. Exposure to deprivation on event-related potentials elicited by visual smoking-relevant cues: effects on desire to smoke and topo- smoking cues. Psychopharmacology 2001; 154: 282–91. graphical components of smoking behavior. Addict Behav 25. Payne T. J., Smith P.O., Sturges L. V., Holleran S. A. Reactiv- 1991; 16: 467–79. ity to smoking cues: mediating roles of nicotine dependence 7. Perkins K. A., Grobe J. E. Increased desire to smoke during and duration of deprivation. Addict Behav 1996; 21: 139– acute stress. Br J Addict 1992; 87: 1037–40. 54. 8. Conklin C. A., Perkins K. A. Subjective and reinforcing 26. Powell J., Dawkins L., Davis R. E. Smoking, reward respon- effects of smoking during negative mood induction. J siveness, and response inhibition: tests of an incentive moti- Abnorm Psychol 2005; 114: 153–64. vational model. Biol Psychiatry 2002; 51: 151–63. 9. Maude-Griffin P. M., Tiffany S. T. Production of smoking 27. Teneggi V.,Tiffany S. T., Squassante L., Milleri S., Ziviani L., urges through imagery. The impact of affect and smoking Bye A. Smokers deprived of cigarettes for 72 hours: effect of abstinence. Exp Clin Psychopharmacol 1996; 4: 198–208. nicotine patches on craving and withdrawal. Psychopharma- 10. Burton S. M., Tiffany S. T. The effect of alcohol consumption cology 2002; 164: 177–87. on craving to smoke. Addiction 1997; 92: 15–26. 28. Tiffany S. T., Cox L. S., Elash C. A. Effects of transdermal 11. Epstein A. M., Sher T. G., Young M. A., King A. C. Tobacco nicotine patches on abstinence-induced and cue-elicited chippers show robust increases in smoking urge after craving in cigarette smokers. J Consult Clin Psychol 2000; alcohol consumption. Psychopharmacology 2007; 190: 68: 233–40. 321–9. 29. Morissette S. B., Palfai T. P., Gulliver S. B., Spiegel D. A., 12. Sayette M. A., Martin C. S., Wertz J. M., Perrott M. A., Peters Barlow D. H. Effects of transdermal nicotine during imagi- A. R. The effects of alcohol on cigarette craving in heavy nal exposure to anxiety and smoking cues in college smokers and tobacco chippers. Psychol Addict Behav 2005; smokers. Psychol Addict Behav 2005; 19: 192–8. 19: 263–70. 30. Waters A. J., Shiffman S., Sayette M. A., Paty J. A., Gwaltney 13. Sayette M. A., Loewenstein G., Kirchner T. R., Travis T. C. J., Balabanis M. H. Cue-provoked craving and nicotine Effects of smoking urge on temporal cognition. Psychol replacement therapy in . J Consult Clin Addict Behav 2005; 19: 88–93. Psychol 2004; 72: 1136–43. 14. Stewart J., deWit H., Eikelboom R. Role of unconditioned 31. Childress A. R., McLellan A. T., O’Brien C. P. Conditioned and conditioned drug effects in the self-administration of responses in a methadone population: a comparison of opiates and stimulants. Psychol Rev 1984; 91: 251–68. laboratory, clinic and natural settings. J Subst Abuse Treat 15. Baker T. B., Morse E., Sherman J. E. The motivation to use 1986; 3: 173–9. drugs: a psychobiological analysis of urges. In: Rivers P. C., 32. Ehrman R. N., Robbins S. J., Childress A. R., O’Brien C. P. editor. The Nebraska Symposium on Motivation: Alcohol and Conditioned responses to -related stimuli in cocaine Addictive Behavior. Lincoln, NE: University of Nebraska abuse patients. Psychopharmacology 1992; 107: 523–9. Press; 1987, p. 257–323. 33. Meyer R. E. Conditioning phenomena and the problem of 16. Bindra D. How adaptive behavior is produced: a perceptual– in opioid addicts and alcoholics. In: Ray R. B., editor. motivational alternative to response–reinforcement. Behav Learning Factors in . Washington, DC: US Brain Sci 1978; 1: 41–91. Department of Health and Human Services; 1988, 161– 17. Neder K., Bechara A., van der Kooy D. Neurobiological 79. constraints on behavioral models of motivation. Annu 34. Piasecki T. M., Smith S. S., Baker T. B. The tyranny of habit Rev Psychol 1997; 48: 85–114. and availability. Addiction 1999; 94: 341–3. 18. Berridge K. C., Robinson T. E. Automatic processes in addic- 35. Wertz J. M., Sayette M. A. A review of the effects of perceived tion: a commentary. In: Wiers R. W., Stacy A. W., editors. drug use opportunity on self-reported urge. Exp Clin Psy- Handbook of Implicit Cognition and Addiction. Thousand chopharmacol 2001; 9: 3–13. Oaks, CA: Sage Publications, Inc.; 2006, p. 477–81. 36. Turkkan J. S., McCaul M. E., Stitzer M. L. Psychophysiologi- 19. Drobes D. J., Tiffany S. T. Induction of smoking urge through cal effects of alcohol-related stimuli: II. Enhancement with imagery and in vivo cue-exposure: physiological and self- alcohol availability. Alcohol Clin Exp Res 1989; 13: 392–8. report manifestations. J Abnorm Psychol 1997; 106: 15–25. 37. Carter B. L., Tiffany S. T. The cue–availability paradigm: the

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 372 Steffani R. Bailey et al.

effects of cigarette availability on cue reactivity in smokers. the natural environment of smokers using ecological Exp Clin Psychopharmacol 2001; 9: 183–90. momentary assessment. Exp Clin Psychopharmacol 2009; 38. Sayette M. A., Wertz J. M., Martin C. S., Cohn J. F., Perrott M. 17: 70–7. A., Hobel J. Effects of smoking opportunity on cue-elicited 42. Tiffany S. T. Drug craving and affect. In: Kassel J., editor. urge: a facial coding analysis. Exp Clin Psychopharmacol Substance Abuse and Emotion. Washington, DC: American 2003; 11: 218–27. Psychological Association; 2009, p. 83–108. 39. Diener E., Emmons R. A. The independence of positive 43. Zinser M. C., Baker T. B., Sherman J. E., Cannon D. S. Rela- and negative affect. J Pers Soc Psychol 1984; 47: 1105– tion between self-reported affect and drug urges and crav- 17. ings in continuing and withdrawing smokers. J Abnorm 40. Shiffman S., Jarvik M. E. Smoking withdrawal symptoms in Psychol 1992; 101: 617–29. two weeks of abstinence. Psychopharmacology 1976; 50: 44. Sayette M. A., Martin C. S., Hull J. G., Wertz J. M., Perrot M. 35–9. A. Effects of nicotine deprivation on craving response cova- 41. Warthen M. W., Tiffany S. T. Evaluation of cue reactivity in riation in smokers. J Abnorm Psychol 2003; 112: 110–18.

© 2009 The Authors. Journal compilation © 2009 Society for the Study of Addiction Addiction, 105, 364–372 This document is a scanned copy of a printed document. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material.