Stereo-EEG reveals rich cortical dynamics in humans coping with difficult action discrimination.

Abstract

Visual perception of others actions is important for social interactions, and the ability to do so, even when one gets only brief glimpses of others behavior, may be crucial for survival. At present it is unknown how the human brain solves this problem. Imaging studies have promoted the idea that the multiple demand (MD) system, a domain general system of the human brain, operates in difficult cognitive and perceptual tasks, but not in tasks in which sensory information is reduced. Functional imaging, based on slow hemodynamic responses, may miss or standardize neural events with very diverse time courses. Here we exploited the temporal resolution of stereo-EEG to study directly cortical activity when human subjects must judge the actions of others, but only get brief glimpses of others activity, because the videos were truncated. Multiple cortical regions increased their activity in the difficult action discrimination, relative to the easy task when the complete video was visible. The majority of these regions belonged to the MD system, being located in parietal or prefrontal cortex. The variety of time courses, lasting from a few 100ms to several seconds, allowed us to disentangle control from effector regions, the latter processing observed actions. This distinction was further supported by relationships with behavior. A key operation within the control clusters was the prediction of erroneous responses, which was initiated in the PPC soon after the end of the truncated video. The time courses further suggested that MD regions not only exert control, but also perform various evaluations of the effort, important for efficient and intelligent behavior. We observed also increases outside the MD system, in temporo-parietal cortex, which may provide contextual information about variables related to the observed action, such as the actor, the object or the scene. Furthermore, to cope with the brief sensory input, the MD system called upon warning regions reacting to the static picture of the actor presented just before the video. We conclude that discrimination of brief observed actions indeed involves the MD system, which is thus is more general than assumed so far. WE also show that the MD system is more complex than assumed, as it includes evaluation of control, and more flexible, as it interacts with other systems than simply the effector circuit of the task.