Skin conductance responses are elicited by the airway sensory effects of puffs from cigarettes

Abstract

The airway sensations stimulated by smoking are an important source of hedonic impact (pleasure) for dependent smokers. The learning process by which these sensations become pleasurable is not well understood. The classical conditioning model predicts that airway sensory stimulation will elicit sympathetic arousal that is positively correlated with the hedonic impact that is elicited by airway sensory stimulation. To test this prediction, we measured skin conductance responses (SCRs) and subjective hedonic impact elicited by a series of individual puffs from nicotinized, denicotinized and unlit cigarettes. Nicotinized puffs elicited more subjective hedonic impact than denicotinized and unlit puffs partly as a result of the fact that they provided a greater level of airway sensory stimulation. We found that SCRs were not larger for nicotinized puffs than for denicotinized puffs, but that they were larger for both nicotinized and denicotinized puffs than for unlit puffs. We also found that the average SCR of a subject to denicotinized puffs was positively correlated with the average hedonic impact that a subject obtained from denicotinized puffs. Together, this suggests that SCR magnitude does not reflect within-subject variations in hedonic impact that are due to variations in the level of airway sensory stimulation, but that it does reflect individual differences in the amount of hedonic impact that is derived from a given level of airway sensory stimulation. The results of a post hoc correlation analysis suggest that these individual differences may have been due to variations in the prevailing urge to smoke. The implications of these findings for the classical conditioning model, as well as for other learning models, are discussed.

Introduction

Cigarette smoking is the most common preventable cause of morbidity and mortality in the developed world (Peto et al., 1992). Cigarette smoking is an addictive behavior, characterized by a compulsion to smoke despite awareness of its negative consequences (American Psychiatric Association, 2001). An accumulating body of evidence from both human and animal models (reviewed in Caggiula et al., 2001) suggests that the sensory context of smoking is important for maintaining dependence. Through learning that depends upon the pharmacologic effects of nicotine, the myriad sensory stimuli that are associated with the act of smoking acquire powerful motivational properties, and so come to drive smoking behavior.

Particularly important for the subjective pleasure, or hedonic impact, obtained from smoking are the airway sensations stimulated by each puff from a cigarette. For example, blocking airway sensation reduces smoking desirability and satisfaction and also the reduction in urge that is obtained from smoking by dependent smokers (Rose et al., 1985, Rose et al., 1999, Rose et al., 1984). Conversely, stimulating airway sensations through inhalation of irritant substances is experienced as desirable and reduces smoking urges in dependent smokers (Behm et al., 1990, Rose and Behm, 1994, Rose and Hickman, 1987). In addition, smoking of cigarettes from which nicotine has been nearly completely removed (denicotinized cigarettes), elicits a number of subjective positive hedonic effects that are actually greater than those elicited by intravenous nicotine administration in dependent smokers (Rose et al., 2000, Westman et al., 1996). In a clinical trial, it has been shown that “replacement” of the airway sensory effects of smoking can more than double the efficacy of nicotine replacement therapy for smoking cessation (Westman et al., 1995). Together, this evidence suggests that airway sensory stimulation is not only pleasurable, but that it is one of the primary goals that dependent smokers achieve by smoking. For this reason, understanding the psychological and neural processes by which airway sensory stimulation gives rise to pleasure may aid the development of more effective treatments for smoking dependence.

It has been proposed that the airway sensory effects of smoking, which are aversive for non-smokers, become pleasurable through repeated association with the pharmacologic effects of nicotine (Rose and Levin, 1991). An extensive literature (reviewed in Childress et al., 1993) has examined how drug-associated cues sensory cues acquire the capacity to elicit motivational states through classical conditioning. In classical conditioning, an initially neutral sensory cue (conditioned stimulus) acquires motivational value through repeated pairing with the pharmacologic effect of a drug (unconditioned stimulus). Through this process, the sensory cue comes to elicit behavioral, subjective and autonomic responses (conditioned responses) that resemble the behavioral, subjective and autonomic responses elicited by the pharmacologic effect of the drug (unconditioned responses). The existence of conditioned responses that are similar the unconditioned responses to the drug provides indirect evidence that the drug cue activates a central state that is similar to the central state elicited by the pharmacologic effects of the drug. Further evidence for this comes from showing that the behavioral, subjective and autonomic responses to drug cues are correlated with each other (Carter and Tiffany, 1999, Glautier and Remington, 1995).

The classical conditioning model has been used primarily as a means to understand the learning process by which previously neutral environmental smoking cues, such as the sight of another person smoking, come to elicit a subjective urge to smoke. The classical conditioning model may also be used to understand how airway sensory effects of smoking can come to elicit subjective pleasure during smoking. According to the classical conditioning model, airway sensory stimulation is a conditioned stimulus that, through repeated association with the pharmacologic effects of nicotine, comes to elicit subjective and autonomic responses that are similar to the pharmacologic effects of nicotine. A large body of literature (reviewed in Kalman, 2002) points to nicotine being a source of subjective pleasure, or positive hedonic impact. Nicotine also elicits an increase in sympathetic arousal (Niedermaier et al., 1993). The classical conditioning model therefore predicts that airway sensory stimulation will elicit both positive hedonic impact and sympathetic arousal. Since these are proposed to arise from the same central state, the classical conditioning model also predicts that the hedonic impact and sympathetic arousal elicited by airway sensory stimulation will be positively correlated with each other.

In this study, we sought to determine whether the airway sensory effects of smoking elicit skin conductance responses (SCRs) and whether the magnitude of these responses is related to the amount of positive hedonic impact that is elicited by the airway sensory effects of smoking. Skin conductance response was chosen because it is a relatively pure measure of sympathetic arousal (Boucsein, 1992). We measured subjective hedonic impact and SCRs elicited by individual puffs from nicotinized, denicotinized and unlit cigarettes. Previous findings have shown that the airway sensory effects of nicotine give rise to hedonic impact (Pritchard et al., 1996, Rose et al., 1999) and that this contributes significantly to the difference in hedonic impact between nicotinized and denicotinized puffs (Naqvi and Bechara, 2005). We therefore predicted that SCR would be larger for nicotinized puffs than for denicotinized and unlit puffs, since more hedonic impact is derived from the airway sensory effects of nicotinized puffs than from the airway sensory effects of denicotinized puffs. We also examined the relationship between individual differences in SCR and individual differences in subjective hedonic impact for nicotinized and denicotinized puffs. Since hedonic impact is derived from airway sensory stimulation for both nicotinized and denicotinized puffs, we predicted that subjects who obtain more hedonic impact from nicotinized and denicotinized puffs would have a higher SCR to nicotinized and denicotinized puffs, respectively.