It's the intention that matters : neural representations of learning from intentional harm in social interactions

As a social species, humans are not only driven by the pursuit of necessities such as food and shelter, but also complex processes such as social interactions. To navigate our everyday life, we use information gathered throughout a lifetime of social interactions in which we learn from others and their actions but also, and not less importantly, about others. To create a complete picture of a social interaction, we assess the individual we interact with, make judgements about them and their actions, and integrate what we know with the consequences of their actions. This way, we learn the relationship between events (e.g. others’ actions) and environmental stimuli, such as other individuals that predict the actions. As we encounter more people and go through more interactions, we continuously update information stored in memory from previous experiences. A common task, for example, going through the busy corridor in our workplace in a hurry does not only include avoiding physical harm caused by bumping into the coffee machine with a sharp corner, but also avoiding a co-worker we are in a feud with, and whom we believed knowingly spilled hot coffee on another co-worker the week before.

How social information is processed is key in understanding rarer but more impactful events that can have lifelong impact on an individual’s life. Interpersonal trauma, a type of trauma that is acquired from harm received from another individual, leads more often to post-traumatic stress disorder (PTSD) than non-socially related trauma, for example, a car crash (Kleim, Ehlers, & Glucksman, 2007). To understand why a specific social harm affect us negatively, it is crucial to study how the brain integrates social, as well as nonsocial (physical) information during the harmful event.

In Study I, II, and III we investigated how different streams of information (social and physical) are integrated during a social interaction. We were interested in how intentionality of an action that has direct aversive consequences on an individual can change the individuals’ judgements of the action and the person performing it. Using a time-based neuroimaging approach, we investigated how the value of an action is integrated with that of the intention behind it. Study I revealed evidence that suggests that intentionality of a directly experienced aversive action is represented throughout the cortex in neural activity patterns that form over time. Study II highlighted the importance of timing and sample size in similar paradigms, and that neural pattern formation in response to aversive actions regardless of the intentions behind them are robustly replicated.

In Study III we asked questions about how these learned action outcomes and knowledge about the people performing the harmful action change neural connectivity, and how this translates into changes in perception and memory 24-hours later. We found an increased connectivity between the hippocampus and the amygdala, which correlated with generalized memory responses to images associated with shocks from an intentional harm do-er, and increased connectivity between the FFA and the insula, as well as the FFA and the dorsomedial prefrontal cortex (dmPFC) correlated with facilitated recognition of the intentional harm do-er’s face.

List of scientific papers

I. Undeger, I., Visser, R. M., & Olsson, A. (2020). Neural Pattern Similarity Unveils the Integration of Social Information and Aversive Learning. Cerebral Cortex. 30(10), 5410-5419.
https://doi.org/10.1093/cercor/bhaa122

II. Undeger, I., Visser, R. M., Becker, N., de Boer, L., Golkar, A., Olsson, A. Model-based representational similarity analysis of BOLD fMRI captures threat learning in social interactions. R Soc Open Sci. 8: 202116.
https://doi.org/10.1098/rsos.202116

III. Undeger, I., Vieira, J. B., Thompson, W., Olsson, A. Brain functional connectivity after social interaction predicts enhanced memory for intentional harm. [Manuscript]