Fear-relevant outcomes modulate the neural correlates of probabilistic classification learning

Although much work has implicated the contributions of frontostriatal and medial temporal lobe (MTL) systems during probabilistic classification learning, the impact of emotion on these learning circuits is unknown. We used a modified version of the weather prediction task in which two participant groups were scanned with identical neutral cue cards probabilistically linked to either emotional (snake/spider) or neutral (mushroom/flower) outcomes. Owing to the differences in visual information shown as outcomes, analyses were restricted to the cue phase of the trials. Learning rates did not differ between the two groups, although the Emotional group was more likely to use complex strategies and to respond more slowly during initial learning. The Emotional group had reduced frontostriatal and MTL activation relative to the Neutral group, especially for participants who scored higher on snake/spider phobia questionnaires. Accurate performance was more tied to medial prefrontal activity in the Emotional group early in training, and to MTL activity in the Neutral group later in training. Trial-by-trial fluctuations in functional connectivity between the caudate and MTL were also reduced in the Emotional group compared to the Neutral group. Across groups, reaction time indexed a switch in learning systems, with faster trials mediated by the caudate and slower trials mediated by the MTL and frontal lobe. The extent to which the caudate was activated early in training predicted later performance improvements. These results reveal insights into how emotional outcomes modulate procedural learning systems, and the dynamics of MTL-striatal engagement across training trials.