Abstract
Persons suffering from anxiety disorders display facilitated processing of arousing and negative stimuli, such as negative words. This memory bias is reflected in better recall and increased amygdala activity in response to such stimuli. However, individual learning histories were not considered in most studies, a concern that we meet here. Thirty-four female persons (half with high-, half with low trait anxiety) participated in a criterion-based associative word-learning paradigm, in which neutral pseudowords were paired with aversive or neutral pictures, which should lead to a valence change for the negatively paired pseudowords. After learning, pseudowords were tested with fMRI to investigate differential brain activation of the amygdala evoked by the newly acquired valence. Explicit and implicit memory was assessed directly after training and in three follow-ups at 4-day intervals. The behavioral results demonstrate that associative word-learning leads to an explicit (but no implicit) memory bias for negatively linked pseudowords, relative to neutral ones, which confirms earlier studies. Bilateral amygdala activation underlines the behavioral effect: Higher trait anxiety is correlated with stronger amygdala activation for negatively linked pseudowords than for neutrally linked ones. Most interestingly, this effect is also present for negatively paired pseudowords that participants could not remember well. Moreover, neutrally paired pseudowords evoked higher amygdala reactivity than completely novel ones in highly anxious persons, which can be taken as evidence for generalization. These findings demonstrate that few word-learning trials generate a memory bias for emotional stimuli, indexed both behaviorally and neurophysiologically. Importantly, the typical memory bias for emotional stimuli and the generalization to neutral ones is larger in high anxious persons.
Highlights
Arousing situations and stimuli are processed preferentially
Voxelwise tests inside the region of interest (ROI) were performed and activity within the amygdalae was correlated with STAI-T scores separately for each subject
Learned pseudowords elicited more amygdala activity than novel pseudowords in the bilateral amygdala, and this effect was positively related to measures of trait anxiety x = 32, y = 5, z = −21, t(32) = 2.62, k = 111 voxels, p = 0.007
Summary
Arousing situations and stimuli are processed preferentially. This has been shown by a vast body of studies, with methods ranging from simple behavioral measures to stateof-the-art imaging techniques (e.g., Junghöfer et al, 2001; Koster et al, 2006; Laeger et al, 2012; Eden et al, 2014; Weierich and Treat, 2015; for a meta-analysis, see Bar-Haim et al, 2007; for a review, see Cisler and Koster, 2010). For a better understanding of this large group of disorders, and for the improvement of therapeutic treatments, it is crucial to understand the mechanisms that underlie the acquisition and processing of arousing-negative stimuli To this aim, we compare persons with high and low (subclinical) anxiety in an associative learning paradigm, using behavioral and neuroimaging measures. Given the ongoing debate about the neurobiological basis of (trait) anxiety, it is crucial to incorporate imaging measurements into the study design, especially when stimuli are presented below threshold, or trained in a shallow learning paradigm that does not guarantee robust explicit access The latter is the case in our study, in which persons with high or low levels of anxiety should learn to associate meaning to pseudowords with only few learning instances.
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