Neural and Behavioral Correlates of Alcohol-Induced Aggression Under Provocation

Abstract

Although alcohol consumption is linked to increased aggression, its neural correlates have not directly been studied in humans so far. Based on a comprehensive neurobiological model of alcohol-induced aggression, we hypothesized that alcohol-induced aggression would go along with increased amygdala and ventral striatum reactivity and impaired functioning of the prefrontal cortex (PFC) under alcohol. We measured neural and behavioral correlates of alcohol-induced aggression in a provoking vs non-provoking condition with a variant of the Taylor aggression paradigm (TAP) allowing to differentiate between reactive (provoked) and proactive (unprovoked) aggression. In a placebo-controlled cross-over design with moderate alcohol intoxication (~0.6 g/kg), 35 young healthy adults performed the TAP during functional magnetic resonance imaging (fMRI). Analyses revealed that provoking vs non-provoking conditions and alcohol vs placebo increased aggression and decreased brain responses in the anterior cingulate cortex/dorso-medial PFC (provokingonon-provoking) and the ventral striatum (alcoholoplacebo) across our healthy sample. Interestingly, alcohol specifically increased proactive (unprovoked) but not reactive (provoked) aggression (alcohol × provocation interaction). However, investigation of inter-individual differences revealed (1) that pronounced alcohol-induced proactive aggression was linked to higher levels of aggression under placebo, and (2) that pronounced alcohol-induced reactive aggression was related to increased amygdala and ventral striatum reactivity under alcohol, providing evidence for their role in human alcohol-induced reactive aggression. Our findings suggest that in healthy young adults a liability for alcohol-induced aggression in a non-provoking context might depend on overall high levels of aggression, but on alcohol-induced increased striatal and amygdala reactivity when triggered by provocation.

Neural Correlates of Aggressive Behavior in Real Time: a Review of fMRI Studies of Laboratory Reactive Aggression

“…Although all studies employed a provocation, retaliation, and an outcome phase, seven studies specifically examined provocation effects on neural activity. Five of these examined the effect of provocation on the decision (retaliation) phase [62•, 64•, 65•, 66•, 67•]; two on the outcome phase [65•, 66•]; and two during the provoking event [61•, 68•]. Seven studies assessed neural correlates of retaliation, although approaches varied (see Table 1).…”

“…Seven studies assessed neural correlates of retaliation, although approaches varied (see Table 1). Three studies included pharmacological manipulations (vasopressin [63•]; tryptophan depletion [62•]; alcohol [68•]) and one examined endogenous hormones [66•]. Studies employed whole-brain analyses, ROI analyses, or both.…”

“…It is worth noting that in most of the studies, the effect of provocation on neural activity was observed during decision-making when subjects were deciding the level of punishment to set for the opponent. Only two of five studies examined provocation independent of decision-making [61•, 68•]. …”

“…Two studies found positive modulation of the insula by provocation [61•, 67•], and one found negative modulation [68•]. Two of these studies observed the activation during stand-alone provocation, while one [67•] observed activation during decision-making.…”

“…In three studies, provocation was found to modulate activity in the thalamus, two positively [61•, 67•] and one negatively [68•]. Located in the diencephalon between cerebral cortex and midbrain, the thalamus acts to relay sensory and motor information between sensory, subcortical (e.g., amygdala) and cortical brain structures.…”