Evidence accumulation and associated error-related brain activity as computationally-informed prospective predictors of substance use in emerging adulthood

Abstract

Substance use peaks during the developmental period known as emerging adulthood (roughly ages 18-25), but not every individual who uses substances during this period engages in frequent or problematic use. Previous studies have suggested that individual differences in neurocognition may prospectively predict problematic substance use, but mechanistic neurocognitive risk factors with clear links to both behavior and neural circuitry have not yet been identified. Here we take an approach rooted in computational psychiatry, an emerging field in which formal models of neurocognition are used to identify candidate biobehavioral dimensions that confer risk for psychopathology. Specifically, we test whether lower efficiency of evidence accumulation (EEA), a computationally tractable process that drives neurocognitive performance across many tasks, is a risk factor for substance use in emerging adults. In an fMRI substudy within a sociobehavioral longitudinal study (n=106), we find that lower EEA and reductions in a robust neural-level correlate of EEA (error-related activations in salience network and parietal structures) measured at ages 18-21 are both prospectively related to higher levels of substance use during ages 22-26, even after adjusting for other well-known risk factors. Results from Bayesian model comparisons corroborated inferences from conventional hypothesis testing and provided evidence that both EEA and its neural correlates contain unique predictive information about substance use involvement. Overall, these findings suggest that EEA is a mechanistic, computationally tractable neurocognitive risk factor for substance use at a critical developmental period, with clear links to both neural correlates and well-established formal theories of brain function.

Task-general efficiency of evidence accumulation as a computationally-defined neurocognitive trait: Implications for clinical neuroscience

“…Beyond research on ADHD, reductions in EEA have been documented in schizophrenia (126,127), depression (128), individuals at risk for frequent substance use (129), and individuals with high levels of externalizing spectrum symptoms (130). Extending these findings, our recent work has provided direct evidence that EEA is a transdiagnostic risk factor for psychopathology (131).…”

Impaired Evidence Accumulation as a Transdiagnostic Vulnerability Factor in Psychopathology

“…This prediction could be tested in future studies, for example developmental studies that measure EEA in youth prior to the onset mental disorders. In recent studies 76,77 , we measured EEA in young adults in a Go/No Go task. We found EEA was significantly (inversely) associated externalizing symptoms 76 and, importantly, was prospectively related with later substance use severity 77 , providing some initial evidence for this second prediction.…”

Sex differences in distributed error-related neural activation in binge drinking young adults

“…Measures of alcohol consumption, alcohol problems, cannabis use, illicit drug use, and a self-report measure of impulsivity were also collected. We replicated our previous methods by forming a multivariate summary measure (the first component from a principal component analysis) of error-related activation across an array of distributed brain regions associated with error monitoring and the salience network (Weigard et al, 2021). Based on prior research, we expected that females would have greater error-related neural activation, as indexed by this multivariate summary measure, compared to males.…”

“…An event-related go/no-go task (e.g., Cope et al, 2020;Durston et al, 2002;Hardee et al, 2014;Heitzeg et al, 2014Heitzeg et al, , 2010Weigard et al, 2021) was used to assess brain activation during false alarms (i.e., pressing the button during a "no-go" stimulus). Participants were instructed to respond via button press to "go" stimuli (all letters except for "X"; 75% of stimuli) but withhold their response to "no-go" stimuli (letter "X"; 25% of stimuli).…”

“…These results are consistent with theoretical models positing that the ACC and anterior insula are central nodes in a "salience network" that supports goal-directed behavior by monitoring task-relevant events (such as errors) and engaging cognitive control processes in response to them (Menon & Uddin, 2010;Seeley et al, 2007). Representative of models of error monitoring's importance for goal-directed behavior, reduced salience network and prefrontal responses to errors during behavioral tasks have been linked to greater substance use and related externalizing behavior (Aharoni et al, 2013;Campanella et al, 2017) and have been found to prospectively predict substance use in longitudinal data (Heitzeg et al, 2014;Weigard et al, 2021). Taken together, this body of work suggests that neural responses to errors reflect the stability of brain systems involved in facilitating cognitive control and goal-directed behavior through the monitoring of errors and other task-relevant events.…”