Mental Representations Mediate Aversive Learning in Humans

Mental representations of stimuli that are not physically present are critical for a range of cognitive capacities, including perception, memory, and learning. Overly robust mental representations, however, can contribute to hallucinations in healthy individuals and those diagnosed with psychotic illness. Measuring the strength of mental representations can thus provide insight into how the contents of the mind influence both adaptive and maladaptive behaviors. In rodents, the robustness of mental representations has been tested using the representation-mediated learning (RML) task, in which animals respond less to a cue after a stimulus that has previously been associated with this cue has been paired with illness. This suggests that the mental representation of the cue enters into a negative association during aversive learning, even though the cue is not physically present. Here, we developed a human version of the RML task in which participants initially learned associations between two visual symbols and two different appetitive food odors. Preference for the food odors was then tested immediately before and after a session in which one symbol was paired with an aversive noise. We observed that mediated learning, in the form of selective decrease in preference for the odor previously paired with the noise-predicting symbol, was directly proportional to direct aversive learning for the symbols themselves. These findings suggest that a mental representation of the odor entered into a negative association with the sound and pave the way for future studies aimed at characterizing the neural circuits of mediated learning in the human brain.