Transfer of incentive salience from a first‐order alcohol cue to a novel second‐order alcohol cue among individuals at risk for alcohol use disorder: electrophysiological evidence

Abstract

Background and aimsIn susceptible individuals, cues associated with drug use are theorized to take on incentivemotivational properties, including the ability to reinforce higher-order, drug-related associative learning. This study aimed to test this prediction among people varying in risk for alcohol use disorder. Design, setting and participants Repeatedmeasures experiment with a measured individual difference variable at a University psychology laboratory in Missouri, USA. One hundred and six young adults (96 contributed complete data) were pre-selected to represent the upper and lower quartiles of self-reported sensitivity to alcohol's acute effects. Measurements Participants completed a second-order Pavlovian conditioning paradigm in which an initially neutral visual cue (second-order conditional stimulus; CS 2 ) predicted onset of an olfactory cue (first-order conditional stimulus; CS 1 ). Olfactory cues were isolated from alcoholic beverages, sweets and non-comestible substances, each presumed to have a natural history of first-order conditioning. Event-related potential responses to the CS 2 across its conditioning and extinction, and to the CS 1 , provided neurophysiological indices of incentive salience (IS). Findings The IS of the alcohol CS 1 was higher among participants low in alcohol sensitivity (LS), relative to their higher-sensitivity (HS) peers. The IS of the CS 2 paired with the alcohol CS 1 increased across the CS 2 conditioning phase among LS but not HS participants. Also, LS (but not HS) individuals also experienced increases in alcohol craving following alcohol CS 1 exposure, and this change was correlated with increases in the IS of the CS 2 paired with the alcohol CS 1 . Conclusions Alcoholic beverage odor, a proximal cue for alcohol consumption, appears to reinforce conditioning of neurophysiological responses to a novel cue among low alcohol sensitivity (LS) individuals but not high alcohol sensitivity individuals, providing the first evidence that the LS phenotype may be associated with differences in the conditioned reinforcing properties of alcohol-related cues. These findings support the idea that the LS phenotype may increase alcohol use disorder risk via susceptibility to incentive salience sensitization.

Internal consistency and test–retest reliability of the P3 event‐related potential (ERP) elicited by alcoholic and non‐alcoholic beverage pictures

“…Enhanced ACR-P3 is associated with heavier and more hazardous alcohol use (Herrmann et al, 2001;Kroczek et al, 2018;Petit et al, 2013) as well as lower self-reported sensitivity to the acute effects of alcohol (Bartholow et al, 2007(Bartholow et al, , 2010, especially its sedative-like effects (Martins et al, 2019). Lower sensitivity to alcohol itself is associated with heavier and more hazardous alcohol use including use-related negative consequences and alcohol use disorder (AUD) symptoms (Bailey & Bartholow, 2016;Bartholow et al, 2007Bartholow et al, , 2010Davis et al, 2021;Fleming & Bartholow, 2014;Fleming et al, 2021;Hone et al, 2017;Martins et al, 2019;Trela et al, 2016), providing converging evidence for the association between enhanced ACR-P3 and AUD risk. Enhanced ACR-P3 also predicts heavier alcohol use prospectively (Bartholow et al, 2007) and differentiates individuals with AUD from those without (Namkoong et al, 2004).…”

“…Recently, there has been growing interest in the possibility that enhancement of various ERP components elicited by alcohol and drug-related cues could index risk that is more specific to alcohol and drug use. In particular, researchers have focused on neurocognitive processes related to the salience of alcohol and drug-related cues , such as selective attention (e.g., Dickter et al, 2014;Kroczek et al, 2018;Petit et al, 2012;Shin et al, 2010) and incentive-motivational value (e.g., Deweese et al, 2018;Dunning et al, 2011;Fleming et al, 2021;Garland et al, 2019;Minnix et al, 2013;Piasecki et al, 2017). Of special interest are the P3 and LPP components, established over half a century of work in experimental psychophysiology as indicators of extrinsic and intrinsic incentive-motivational value attributed to the eliciting stimulus (e.g., Begleiter et al, 1983;Codispoti et al, 2021;Deweese et al, 2016;Franken et al, 2011;Schindler & Straube, 2020;Schupp et al, 2000; for review, see: Hajcak & Foti, 2020).…”

“…In particular, enhanced P3/LPP response to alcoholrelated relative to non-alcohol cues (alcohol cue reactivity P3/LPP; henceforth: the ACR-P3) has been posited as an indicator of individual differences in the attribution of incentive-motivational value, an aspect of emotional significance, to alcohol-related cues (e.g., Fleming et al, 2021;Herrmann et al, 2001;Kroczek et al, 2018). Enhanced ACR-P3 is associated with heavier and more hazardous alcohol use (Herrmann et al, 2001;Kroczek et al, 2018;Petit et al, 2013) as well as lower self-reported sensitivity to the acute effects of alcohol (Bartholow et al, 2007(Bartholow et al, , 2010, especially its sedative-like effects (Martins et al, 2019).…”

Alcohol craving in the natural environment: Moderating roles of cue exposure, drinking, and alcohol sensitivity.

“…Identifying alcohol-use phenotypes associated with susceptibility to incentive salience sensitization (ISS) is an important translational goal. Evidence from both rodents (e.g., Beckstead & Phillips, 2009;Murphy et al, 2002;Risinger et al, 1994) and humans (see Cofresí et al, 2019Cofresí et al, , 2021Fleming et al, 2021) suggests low sensitivity (LS) to alcohol's acute effects (i.e., requiring a larger dose to experience various effects)a heritable, biobehavioral trait (Heath et al, 1999;Ray, Miranda, et al, 2010;Viken et al, 2003) linked to increased AUD risk (e.g., Schuckit, 1994; also see King et al, 2014King et al, , 2021, for evidence that higher sensitivity to alcohol's stimulating effects predicts AUD onset)-as a promising candidate phenotype associated with ISS susceptibility.…”

“…Two recent studies tested this idea. In a sample of underage drinkers, Fleming et al (2021) found that exposure to This document is copyrighted by the American Psychological Association or one of its allied publishers.…”