Binge drinking is associated with attenuated frontal and parietal activation during successful response inhibition in fearful context

Abstract

Binge drinking is associated with increased impulsivity and altered emotional processing. This study investigated, in a group of university students who differed in their level of binge drinking, whether the ability to inhibit a pre-potent response and to delay gratification is disrupted in the presence of emotional context. We further tested whether functional connectivity within intrinsic resting-state networks was associated with alcohol use. Higher incidence of binge drinking was associated with enhanced activation of the lateral occipital cortex, angular gyrus, the left frontal pole during successful response inhibition irrespective of emotional context. This observation suggests a compensatory mechanism. However, higher binge drinking attenuated frontal and parietal activation during successful response inhibition within a fearful context, indicating the selective emotional facilitation of inhibitory control. Similarly, higher binge drinking was associated with attenuated frontopolar activation when choosing a delayed reward over an immediate reward within the fearful, relative to the neutral, context. Resting-state functional data analysis revealed that binge drinking decreased coupling between the right supramarginal gyrus and Ventral Attention Network, indicating alcohol-associated disruption of functional connectivity within brain substrates directing attention. Together, our results suggest that binge drinking makes response inhibition more effortful, yet emotional (more arousing) contexts may mitigate this; disrupted functional connectivity between regions underlying adaptive attentional control, is a likely mechanism underlying these response inhibition effects associated with binge drinking.

Disrupted Fear and Sadness Recognition in Binge Drinking: A Combined Group and Individual Analysis

“…First, it has been suggested that amygdala lesions may lead to impaired fear processing (Morris et al., ) and this proposal has been supported in SAUDs (e.g., Donadon and Osório, ; O'daly et al., ; Salloum et al., ; Townshend and Duka, ). In binge drinking, amygdala dysfunctions have also been observed (Stephens and Duka, ; Xiao et al., ) and some studies reported impairments in fear processing in preclinical (Stephens et al., ) and human (Herman et al., ) studies. The current results are thus in line with previous ones (Herman et al., ; Stephens et al., ) by showing that BD have difficulties to recognize fearful facial expressions.…”

“…In binge drinking, amygdala dysfunctions have also been observed (Stephens and Duka, ; Xiao et al., ) and some studies reported impairments in fear processing in preclinical (Stephens et al., ) and human (Herman et al., ) studies. The current results are thus in line with previous ones (Herman et al., ; Stephens et al., ) by showing that BD have difficulties to recognize fearful facial expressions. Importantly, the processing of fear is identified as fundamental in the widely known dichotomy between approach and avoidance behaviors (Marsh et al., ).…”

Addiction in focus: molecular mechanisms, model systems, circuit maps, risk prediction and the quest for effective interventions

“…Neuroimaging was used to study the neural correlates of the core cognitive and emotional impairments in drug addiction, similar to the ones emphasized in the iRISA (impaired response inhibition and salience attribution) model (Goldstein & Volkow, , ). For example, in populations at risk (binge drinking university students), evidence was presented for the need for more effort expenditure during response inhibition, as associated with disrupted functional connectivity between regions underlying adaptive attentional control; the suggestion that emotional (more arousing) contexts may mitigate this effect has clear therapeutic implications (Herman et al ., ). Drug‐cue reactivity was studied in another sample of young problem drinkers where the finding of a differential sex (and severity) effect for processing alcohol cues in the striatum (less cue reactivity in females and those with lower alcohol use severity) has implications for both treatment and study design.…”

Binge Drinking and Memory in Adolescents and Young Adults

“…This risk has been suggested to be linked to executive deficits (e.g., [5]). The BD pattern of consumption seems to be especially associated with increased impulsivity and inhibitory control deficits (e.g., [6][7][8]). At the same time, this seems to be due to an attenuated frontal activation (e.g., [8,9]).…”

“…The BD pattern of consumption seems to be especially associated with increased impulsivity and inhibitory control deficits (e.g., [6][7][8]). At the same time, this seems to be due to an attenuated frontal activation (e.g., [8,9]). Thus, a higher incidence of BD has been related to decreased activation of dorsolateral prefrontal cortex, dorsomedial prefrontal cortex, and anterior cingulate cortex, brain regions strongly implicated in executive functioning [9].…”