Extraction of situational meaning by integrating multiple meanings in a complex environment: a functional MRI study

Humans extract behaviorally significant meaning from a situation by integrating meanings from multiple components of a complex daily environment. To determine the neural underpinnings of this ability, the authors performed functional magnetic resonance imaging of healthy subjects while the latter viewed naturalistic scenes of two people and an object, including a threatening situation of a person being attacked by an offender with an object. The authors used a two-factorial design: the object was either aversive or nonaversive, and the offender's action was either directed to the person or elsewhere. This allowed the authors to examine the neural response to object aversiveness and person-directed intention separately. A task unrelated to threat was also used to address incidental (i.e., subconscious or unintentional) detection. Assuming individual differences in incidental threat detection, the authors used a functional connectivity analysis using principal components analysis of intersubject variability. The left lateral orbitofrontal cortex and medial prefrontal cortex (MPFC) were specifically activated in response to a threatening situation. The threat-related component of intersubject variability was extracted from these data and showed a significant correlation with personality scores. There was also a correlation between threat-related intersubject variability and activation for object aversiveness in the left temporal pole and lateral orbitofrontal cortex; person-directed intention in the left superior frontal gyrus; threatening situations in the left MPFC; and independently for both factors in the right MPFC. Results demonstrate independent processing of object aversiveness and person-directed intention in the left temporal-orbitofrontal and superior frontal networks, respectively, and their integration into situational meaning in the MPFC.