Aversive Learning Modulates Cortical Representations of Object Categories

Abstract

Experimental studies of conditioned learning reveal activity changes in the amygdala and unimodal sensory cortex underlying fear acquisition to simple stimuli. However, real-world fears typically involve complex stimuli represented at the category level. A consequence of category-level representations of threat is that aversive experiences with particular category members may lead one to infer that related exemplars likewise pose a threat, despite variations in physical form. Here, we examined the effect of category-level representations of threat on human brain activation using 2 superordinate categories (animals and tools) as conditioned stimuli. Hemodynamic activity in the amygdala and category-selective cortex was modulated by the reinforcement contingency, leading to widespread fear of different exemplars from the reinforced category. Multivariate representational similarity analyses revealed that activity patterns in the amygdala and object-selective cortex were more similar among exemplars from the threat versus safe category. Learning to fear animate objects was additionally characterized by enhanced functional coupling between the amygdala and fusiform gyrus. Finally, hippocampal activity co-varied with object typicality and amygdala activation early during training. These findings provide novel evidence that aversive learning can modulate category-level representations of object concepts, thereby enabling individuals to express fear to a range of related stimuli.

Motivational Salience Modulates Early Visual Cortex Responses across Task Sets

“…Such efficient implementation of feature-based attention could be at the base of transferability of motivational value to new materials. More specifically, these results suggest a representation of threat-related features already in early visual cortex, possibly mediating generalization of behavioral responses in new environments (Dunsmoor, Kragel, Martin, & LaBar, 2013). This in turn could be at the foundation of processes such as the generalization of fear (Dunsmoor, Prince, Murty, Kragel, & LaBar, 2011;Onat & Büchel, 2015), and could explain why anxiety maintenance can be sustained by attentional and perceptual biases also involving coarse visual mechanisms (Rossi & Pourtois, 2013).…”

Fear Generalization in Humans: Systematic Review and Implications for Anxiety Disorder Research

“…Trial-by-trial ratings of shock expectancy and conditioned SCRs confirmed that subjects generalized learning to the category level, treating novel exemplars from the CS+ category as potential threats and novel exemplars from the CS-category as safe. Functional MRI results showed that activity in category-selective regions in the occipitotemporal cortex was modulated as a function of learning history (Dunsmoor, Kragel, Martin, & LaBar, 2013). That is, lateral fusiform gyrus (animal-preferring cortex) activity was enhanced in response to images of animals in subjects for whom animals predicted shock versus subjects for whom this category was safe; whereas activity in the medial fusiform gyrus (tool-preferring cortex) showed the reverse pattern of activity in these subjects (enhanced in subjects for whom tools predicted shock versus subjects for whom tools were safe).…”

Influence of reward motivation on human declarative memory

“…Much like for aversive conditioning (e.g. Dunsmoor et al, 2009Dunsmoor et al, , 2012Dunsmoor et al, , 2013Maren et al, 2013), generalization of reward conditioning may partly rely on physical properties of the stimuli. Conditioned responses (CRs) can extend to stimuli that resemble the CS+ along some basic perceptual dimensions, such as tone pitch, size, or color (Honig and Urcuioli, 1981), or generalize to stimuli sharing more abstract characteristics, such as belonging to a specific visual category like 'cars' or 'flowers' (Bhatt et al, 1988).…”