State-Dependent TMS Reveals Representation of Affective Body Movements in the Anterior Intraparietal Cortex

• Published in: The Journal of neuroscience 2017-07, Vol.37 (30), p.7231-7239
• Main Authors: Mazzoni, Noemi, Jacobs, Christianne, Venuti, Paola, Silvanto, Juha, Cattaneo, Luigi
• Format: Article
• Language: English
• Subjects: Adaptation; Adapters; Adult; Affect - physiology; Arousal - physiology; Brodmann's area; Emotions; Emotions - physiology; Fear - physiology; Female; Happiness; Humans; Information processing; Intraparietal sulcus; Male; Motion detection; Movement; Movement - physiology; Parietal Lobe - physiology; Representations; Superior temporal sulcus; Temporal cortex; Transcranial Magnetic Stimulation; Visual cortex; Visual Perception - physiology
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.0913-17.2017

In humans, recognition of others' actions involves a cortical network that comprises, among other cortical regions, the posterior superior temporal sulcus (pSTS), where biological motion is coded and the anterior intraparietal sulcus (aIPS), where movement information is elaborated in terms of meaningful goal-directed actions. This action observation system (AOS) is thought to encode neutral voluntary actions, and possibly some aspects of affective motor repertoire, but the role of the AOS' areas in processing affective kinematic information has never been examined. Here we investigated whether the AOS plays a role in representing dynamic emotional bodily expressions. In the first experiment, we assessed behavioral adaptation effects of observed affective movements. Participants watched series of happy or fearful whole-body point-light displays (PLDs) as adapters and were then asked to perform an explicit categorization of the emotion expressed in test PLDs. Participants were slower when categorizing any of the two emotions as long as it was congruent with the emotion in the adapter sequence. We interpreted this effect as adaptation to the emotional content of PLDs. In the second experiment, we combined this paradigm with TMS applied over either the right aIPS, pSTS, and the right half of the occipital pole (corresponding to Brodmann's area 17 and serving as control) to examine the neural locus of the adaptation effect. TMS over the aIPS (but not over the other sites) reversed the behavioral cost of adaptation, specifically for fearful contents. This demonstrates that aIPS contains an explicit representation of affective body movements. In humans, a network of areas, the action observation system, encodes voluntary actions. However, the role of these brain regions in processing affective kinematic information has not been investigated. Here we demonstrate that the aIPS contains a representation of affective body movements. First, in a behavioral experiment, we found an adaptation after-effect for emotional PLDs, indicating the existence of a neural representation selective for affective information in biological motion. To examine the neural locus of this effect, we then combined the adaptation paradigm with TMS. Stimulation of the aIPS (but not over pSTS and control site) reversed the behavioral cost of adaptation, specifically for fearful contents, demonstrating that aIPS contains a representation of affective body movements.