From Architecture to Evolution: Multisensory Evidence of Decentralized Emotion

Emotional appraisal in humans is often considered a centrally mediated process by which sensory signals, void of emotional meaning, are assessed by integrative brain structures steps removed from raw sensation. We review emerging evidence that the emotional value of the environment is coded by nonvisual sensory systems as early as the sensory receptors and that these signals inform the emotional state of an organism independent of sensory cortical processes. We further present evidence for cross-species conservation of sensory projections to central emotion-processing brain regions. Based on this, we argue not only that emotional appraisal is a decentralized process, but that all human emotional experience may reflect the sensory experience of our ancestors. Emotions function to motivate adaptive patterns of behavior and cognition, increasing the chance of an organism’s survival and reproduction by allowing it to compare objects, events, and cognitions in a modality-general manner.Current theories of human emotion appraisal as a centrally mediated process neglect evidence from nonvisual modalities, indicating that sensory afferents can reflect the adaptive value of external objects.In humans, valence-coded sensation informs modality-general representations of emotion and well-being independent of modality-specific processing.Whereas emotion processing in humans is predominantly informed by processed cortical signals, emotional processing in many non-human species is characterized by responsivity to raw sensation.We propose that centralized human emotion-processing structures are the evolutionary descendants of regions once dedicated to interpreting valenced-sensation, with valenced sensory inputs an artifact of this developmental history.