We observed that smokers exhibited greater striatal recruitment than nonsmokers during the anticipation of immediate relative to equally preferred delayed rewards. Post hoc analysis of signal change within these regions indicated that the effect was driven by low activation among smokers (relative to nonsmokers) during anticipation of delayed rewards, with no indication of high activation (again relative to nonsmokers) during anticipation of immediate rewards.
We did not observe greater delay discounting among smokers relative to nonsmokers. Although there are several reports in the literature indicating an association between smoking and delay discounting (reviewed above), a null finding is only moderately surprising given effect sizes reported. If the true effect size in the population is D = .65 (the median of those reviewed in Gottdiener et al., 2008
), then null findings would be expected approximately 25% of the time given our sample size (and indeed, given the “file drawer problem,” it is likely that the true effect-size is less than .65). Indeed two of the three studies previously reporting an association between smoking severity and steeper discounting did not observe statistically significant group differences between smokers and nonsmokers (Heyman and Gibb, 2006
; Ohmura et al., 2005
). In the present study, we observed marginal evidence (p=.06) consistent with the same association between severity of dependence and steeper discounting. It is likely that variability in severity of smokers included across studies is an important source of variability in findings regarding discounting behavior in smokers vs. nonsmokers. It is noteworthy that some participants that we identified as nicotine dependent (based on the M.I.N.I.) scored low on the Fagerström Test for Nicotine Dependence. These measures emphasize different features, and lack of correspondence has been previously reported. Indeed, in a large sample, Moochan and colleagues (2002) reported that 24 of 216 individuals that met DSM criteria for nicotine dependence (11.1%) scored 0 or 1 on the Fagerström. The general pattern observed in our data suggests an overall group difference in delay discounting would likely be observed in a similar sample restricted to more severely dependent smokers.
The fact that intertemporal choices tend to be more farsighted than would be expected based on brain response to anticipated immediate and delayed rewards suggests an underlying disposition favoring immediate rewards (or neglecting delayed rewards) that goes beyond what is expressed in delay discounting tasks. Among smokers, the data indicated that striatal response was, relative to comparison participants, abnormally low during the anticipation of delayed rewards. It is possible that this represents dispositional phenotypic variance relevant to initiation or escalation of cigarette smoking. It is also possible that chronic cigarette smoking and/or acute smoking causes the observed effect. Acute nicotine administration enhances phasic responses to rewarding stimuli (Rice and Cragg, 2004
) and lowers intracranial self-stimulation thresholds (Bauco and Wise, 1994
). The effects of chronic nicotine administration on striatal reward response are complex and appear to include both a lowering of striatal D1 and D2 receptor availability (Dagher et al., 2001
; Fehr et al., 2008
), but also evidence of sustained hypersensitivity of the reward system (Kenny and Markou, 2005
; Mansvelder and McGehee, 2000
). The observed pattern of generally lower signal change in relation to monetary reward among smokers is consistent with prior reports based on Positron Emission Tomography. Martin-Soelch and colleagues (2001
) reported data suggestive of hyporesponsiveness in non-abstinent smokers to rewards relative to nonsmokers, especially within the striatum. It should be noted though, that our own data do not include statistical evidence of a group difference in response to immediate rewards.
Interestingly, it was recently reported that acute administration of L-Dopa (which increases dopamine release) was associated with an increased preference for immediate over delayed reward, and with increased attenuation of reward response as a function of delay in brain regions associated with discounting, including the striatum (Pine et al., 2010
). It therefore seems possible that neuroadaptations associated with chronic smoking reduce striatal anticipatory response to delayed rewards, as observed in the present study.
While the significance of revealed preference with regard to addictive behavior is conceptually straightforward, the significance of anticipatory response to delayed rewards is not. What difference, one might reasonably ask, does it make if a hypothetical smoker exhibits low striatal response during the anticipation of delayed rewards, if she is nevertheless willing to choose larger delayed over smaller immediate rewards? One possibility is that low striatal response to delayed rewards represents an underlying disposition that may be expressed when trade-offs are less explicit, or when decision-making is compromised. While real-world choices that entail some trade-off between more and less immediate utility are ubiquitous, the trade-offs are rarely so explicit as they are in intertemporal choice experiments (what exactly is the cost of one cigarette, for example, and when is that cost borne?). There is evidence that discounting tends to be steeper when the trade-off is less easy to quantify than it is in money choice experiments (Chapman, 1996
; Chapman and Elstein, 1995
). There is also evidence that discounting tends to increase when participants are distracted (Mischel et al., 1972
), under working memory load (Hinson et al., 2003
), sexually aroused (Wilson and Daly, 2004
), or in nicotine withdrawal (Field et al., 2006
). One possibility, therefore, is that anticipatory responses to delayed reward may reveal an underlying tendency that is manifested during the less “tangible” (Rick and Loewenstein, 2008
) trade-offs between reward magnitude and immediacy entailed in everyday choice, and or that is revealed when decision-making resources are compromised. If this is the case, the observed finding may play an important role in understanding variability in response among smokers to rational incentives favoring smoking cessation.