Social Cognitive and Addiction Neuroscience Lab (SCANlab)

Research in the SCANlab

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Salience, Cognitive Control, and Social Behavior

The interaction of salience and cognitive control is an enduring area of interest in the SCANlab, going back to Dr. Bartholow’s undergraduate days. In his undergraduate senior honors thesis, Dr. Bartholow found that participants asked to read résumés later recalled more gender-inconsistent information about job candidates. This general theme carried through to Dr. Bartholow’s dissertation research, in which he used event-related brain potentials (ERPs) to examine the neurocognitive consequences of expectancy violations. In that study, expectancy-violating behaviors elicited a larger P3-like positivity in the ERP and were recalled better compared to expectancy-consistent behaviors (Bartholow et al., 2001, 2003). Back then, we interpreted this effect as evidence for context updating (the dominant P3 theory at the time). As theoretical understanding of the P3 has evolved, we now believe this finding reflects the fact that unexpected information is salient, prompting engagement of controlled processing (see Nieuwenhuis et al., 2005 ).

Our research has been heavily influenced by cognitive neuroscience models of the structure of information processing, especially the continuous flow model (Coles et al., 1985; Eriksen & Schultz, 1979) and various conflict monitoring theories (e.g., Botvinick et al., 2001; Shenhav et al., 2016). In essence, these models posit (a) that information about a stimulus accumulates gradually as processing unfolds, and (b) as a consequence, various stimulus properties or contextual features can energize multiple, often competing responses simultaneously, leading to a need to engage cognitive control to maintain adequate performance. This set of basic principles has influenced much of our research across numerous domains of interest (see Bartholow, 2010).

Applied to social cognition, these models imply that responses often classified as “automatic” (e.g., measures of implicit attitudes) might be influenced by control. We first tested this idea in the context of a racial categorization task in which faces were flanked by stereotype-relevant words (Bartholow & Dickter, 2008). In two experiments, we found that race categorizations were faster when faces appeared with stereotype-congruent versus –incongruent words, especially when stereotype-congruent trials were more probable. Further, the ERP data showed that that this effect was not due to differences in the evaluative categorization of the faces (P3 latency), but instead reflected increased response conflict (N2 amplitude) due to partial activation of competing responses (lateralized readiness potential; LRP) on stereotype-incongruent trials. A more recent, multisite investigation (funded by the National Science Foundation) extended this work by testing the role of executive cognitive function (EF) in the expression of implicit bias. Participants (N = 485) completed a battery of EF measures and, a week later, a battery of implicit bias measures. As predicted, we found that expression of implicit race bias was heavily influenced by individual differences in EF ability (Ito et al., 2015). Specifically, the extent to which bias expression reflected automatic processes was reduced as a function of increases in general EF ability.

Another study demonstrating the role of conflict and control in “implicit” social cognition was designed to identify the locus of the affective congruency effect (Bartholow et al., 2009), wherein people are faster to categorize the valence of a target if it is preceded by a valence-congruent (vs. incongruent) prime. This finding traditionally has been explained in terms of automatic spreading of activation in working memory (e.g., Fazio et al., 1986). By measuring ERPs while participants completed a standard evaluative priming task, we showed (a) that incongruent targets elicit response conflict; (b) that the degree of this conflict varies along with the probability of congruent targets, such that (c) when incongruent targets are highly probable, congruent targets elicit more conflict (also see Bartholow et al., 2005); and (d) that this conflict is localized to response generation processes, not stimulus evaluation.

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Salience, Cognitive Control, and Alcohol

Drinking alcohol is inherently a social behavior. Alcohol commonly is consumed in social settings, possibly because it facilitates social bonding and group cohesion (Sayette et al., 2012). Many of the most devastating negative consequences of alcohol use and chronic heavy drinking also occur in the social domain. Theorists have long posited that alcohol’s deleterious effects on social behavior stem from impaired cognitive control. Several of our experiments have shown evidence consistent with this idea, in that alcohol increases expression of race bias due to its impairment of control-related processes (Bartholow et al., 2006, 2012).

But exactly how does this occur? One answer, we believe, is that alcohol reduces the salience of events, such as a control failure (i.e., an error), that normally spur efforts at increased control. Interestingly, we found (Bartholow et al., 2012) that alcohol does not reduce awareness of errors, as others had suggested (Ridderinkhof et al., 2002), but rather reduces the salience or motivational significance of errors. This, in turn, hinders typical efforts at post-error control adjustment. Later work further indicated that alcohol’s control-impairing effects are limited to situations in which control has already failed, and that recovery of control following errors takes much longer when people are drunk (Bailey et al., 2014). Thus, the adverse consequences people often experience when intoxicated might stem from alcohol’s dampening of the typical “affect alarm,” seated in the brain’s salience network (anterior insula and dorsal anterior cingulate cortex), which alerts us when control is failing and needs to be bolstered (Inzlicht et al., 2015).

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Incidental Stimulus Exposure Effects

A fundamental tenet of social psychology is that situational factors strongly affect behavior. Despite recent controversies related to some specific effects, we remain interested in the power of priming, or incidental stimulus exposure, to demonstrate this basic premise. We have studied priming effects in numerous domains, including studies showing that exposure to alcohol-related images or words can elicit behaviors often associated with alcohol consumption, such as aggression and general disinhibition.

Based on the idea that exposure to stimuli increases accessibility of relevant mental content (Higgins, 2011), we reasoned that seeing alcohol-related stimuli might not only bring to mind thoughts linked in memory with alcohol, but also might instigate behaviors that often result from alcohol consumption. As an initial test of this idea, in the guise of a study on advertising effectiveness we randomly assigned participants to view magazine ads for alcoholic beverages or for other grocery items and asked them to rate the ads on various dimensions. Next, we asked participants if they would help us pilot test material for a future study on impression formation by reading a paragraph describing a person and rating him on various traits, including hostility. We reasoned that the common association between alcohol and aggression might lead to a sort of hostile perception bias when evaluating this individual. As predicted, participants who had seen ads for alcohol rated the individual as more hostile than did participants who had seen ads for other products, and this effect was larger among people who had endorsed (weeks previously) the notion that alcohol increases aggression (Bartholow & Heinz, 2006). Subsequently, this finding has been extended to participants’ own aggression in verbal (Friedman et al., 2007) and physical domains (Pedersen et al., 2014), and has been replicated in other labs (e.g., Bègue et al., 2009; Subra et al., 2010).

Of course, aggression is not the only behavior commonly assumed to increase with alcohol. Hence, we have tested whether this basic phenomenon extends into other behavioral domains, and found similar effects with social disinhibition (Freeman et al., 2010), tension-reduction (Friedman et al., 2007), race bias (Stepanova et al., 2012, 2018a, 2018b), and risky decision-making (Carter et al., in prep.). Additionally, it could be that participants are savvy enough to recognize the hypotheses in studies of this kind when alcohol-related stimuli are presented overtly (i.e., experimental demand). Thus, we have also tested the generality of the effect by varying alcohol cue exposure procedures, including the use of so-called “sub-optimal” exposures (i.e., when prime stimuli are presented too quickly to be consciously recognized). Here again, similar effects have emerged (e.g., Friedman et al., 2007; Loersch & Bartholow, 2011; Pedersen et al., 2014).

Taken together, these findings highlight the power of situational cues to affect behavior in theoretically meaningful ways. On a practical level, they point to the conclusion that alcohol can affect social behavior even when it is not consumed, suggesting, ironically, that even nondrinkers can experience its effects.

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Aberrant Salience and Control as Risk Factors for Addiction

Salience is central to a prominent theory of addiction known as incentive sensitization theory (IST; e.g., Robinson & Berridge, 1993). Briefly, IST posits that, through use of addictive drugs, including alcohol, people learn to pair the rewarding feelings they experience (relaxation, stimulation) with various cues present during drug use. Eventually, repeated pairing of drug-related cues with reward leads those cues to take on the rewarding properties of the drug itself. That is, the cues become infused with incentive salience, triggering craving, approach and consummatory behavior.

Research has shown critical individual differences in vulnerability to attributing incentive salience to drug cues, and that vulnerable individuals are at much higher risk for addiction. Moreover, combining incentive sensitization with poor cognitive control (e.g., during a drinking episode) makes for a “potentially disastrous combination” (Robinson & Berridge, 2003, p. 44). To date, IST has been tested primarily in preclinical animal models. Part of our work aims to translate IST to a human model.

In a number of studies over the past decade, we have discovered that a low sensitivity to the effects of alcohol (i.e., needing more drinks to feel alcohol’s effects), known to be a potent risk factor for alcoholism, is associated with heightened incentive salience for alcohol cues. Compared with their higher-sensitivity (HS) peers, among low-sensitivity (LS) drinkers alcohol-related cues (a) elicit much larger neurophysiological responses (Bartholow et al., 2007, 2010; Fleming & Bartholow, in prep.); (b) capture selective attention (Shin et al., 2010); (c) trigger approach-motivated behavior (Fleming & Bartholow, 2014); (d) produce response conflict when relevant behaviors must be inhibited or overridden by alternative responses (Bailey & Bartholow, 2016; Fleming & Bartholow, 2014), and (e) elicit greater feelings of craving (Fleming & Bartholow, in prep.; Piasecki et al., 2017; Trela et al., in press). These findings suggest that LS could be a human phenotype related to sign-tracking, a conditioned response reflecting susceptibility to incentive sensitization and addiction (Robinson et al., 2014).

Recently, our lab has conducted two major projects designed to examine how the incentive salience of alcohol-related cues is associated with underage drinking. One such project, funded by the National Institute on Alcohol Abuse and Alcoholism (NIAAA; R01-AA020970), examined the extent to which pairing beer brands with major U.S. universities enhances the incentive salience of those brands for underage students. Major brewers routinely associate their brands with U.S. universities through direct marketing and by advertising during university-related programming (e.g., college sports). We tested whether affiliating a beer brand with students’ university increases the incentive salience of the brand, and whether individual differences in the magnitude of this effect predict changes in underage students’ alcohol use. We found (a) that P3 amplitude elicited by a beer brand increased when that brand was affiliated with students’ university, either in a contrived laboratory task or by ads presented during university-related sports broadcasts; (b) that stronger personal identification with the university increased this effect; and (c) that variability in this effect predicted changes in alcohol use over one month, controlling for baseline levels of use (Bartholow et al., 2018).

A current project, also funded by the NIAAA (R01-AA025451), aims to connect multiple laboratory-based measures of the incentive salience of alcohol-related cues to underage drinkers’ reports of craving, alcohol use, and alcohol-related consequences as they occur in their natural environments. This project will help us to better understand the extent to which changes in drinking lead to changes in alcohol sensitivity and to corresponding changes in the incentive salience of alcohol-related cues.