Neural representation of emotional valence in human amygdala and surrounding regions

The amygdala is a core structure for encoding the affective value of external stimuli. Animal studies suggest that positive and negative emotions are separately encoded by distinct neuronal populations within the amygdala; however, this hypothesis has rarely been tested in humans. The current study examined this hypothesis by comparing the distributed emotion encoding model, as proposed in animal studies, with the univariate emotion encoding model using functional magnetic resonance (fMRI) imaging. More specifically, we applied univariate regression, using average amygdala activation to represent global activation level, and multivariate regression, using distributed voxel-level pattern within the amygdala, to predict normative valence of affective images from the IAPS library. In the core amygdala, the multivariate model's prediction performance was not better than that of the univariate model, with weight map analysis revealing an overwhelming predominance of voxels selectively responsive to negative stimuli. When the region of interest was expanded to include voxels with lower anatomical probability of belonging to the amygdala as well as voxels from adjacent areas, the multivariate model significantly outperformed the univariate model, with the voxels selectively responsive to positive valence primarily located in regions surrounding the core amygdala. These findings suggest that in the human amygdala, the core region encodes emotional valence primarily through a global activation signal, rather than distributed patterns consisting of separate clusters of positive and negative voxels, and a more distributed valence representation emerges when regions surrounding the amygdala are taken into consideration.