Emotional signals are of pivotal relevance in social interactions. Neuroimaging and lesion studies have established an important role of the amygdala for the processing of these signals. While the human amygdala receives input from all sensory modalities, it is the visual modality that is most important for emotional aspects in social interactions. Consequently, amygdala involvement in visual emotional processing has been unequivocally established, whereas its role in auditory emotional processing is less clear. To investigate amygdala involvement in auditory emotional processing, we used functional magnetic resonance imaging in sighted and connatally blind volunteers, the latter of which lack visual experience during development but have outstanding capabilities to process auditory signals, which are their dominant source of information in social interactions. First, we observed a performance advantage of the connatally blind in auditory discrimination tasks that was paralleled by occipital cortex activation, which was not present in the sighted. More importantly, the blind not only showed robust selective activation in the amygdala to fearful and angry compared to neutral voices but also showed stronger activation to those stimuli than sighted participants. Higher amygdala activity for fearful items was further associated with individual performance in the blind, indicating that amygdala activation in the blind is not only driven by blindness per se but also by inter-individual differences in auditory capabilities. Our results indicate that the responsivity of the amygdala to emotional signals develops even in the absence of visual emotional experience and serves the sensory modality which is the most reliable source of emotional information.
Emotional signals are of pivotal relevance in social interactions. Neuroimaging and lesion studies have established an important role of the amygdala for the processing of these signals. While the human amygdala receives input from all sensory modalities, it is the visual modality that is most important for emotional aspects in social interactions. Consequently, amygdala involvement in visual emotional processing has been unequivocally established, whereas its role in auditory emotional processing is less clear. To investigate amygdala involvement in auditory emotional processing, we used functional magnetic resonance imaging in sighted and connatally blind volunteers, the latter of which lack visual experience during development but have outstanding capabilities to process auditory signals, which are their dominant source of information in social interactions. First, we observed a performance advantage of the connatally blind in auditory discrimination tasks that was paralleled by occipital cortex activation, which was not present in the sighted. More importantly, the blind not only showed robust selective activation in the amygdala to fearful and angry compared to neutral voices but also showed stronger activation to those stimuli than sighted participants. Higher amygdala activity for fearful items was further associated with individual performance in the blind, indicating that amygdala activation in the blind is not only driven by blindness per se but also by inter-individual differences in auditory capabilities. Our results indicate that the responsivity of the amygdala to emotional signals develops even in the absence of visual emotional experience and serves the sensory modality which is the most reliable source of emotional information.