Parallel processing streams for motor output and sensory prediction during action preparation

• Published in: Journal of neurophysiology Vol. 113; no. 6; pp. 1752 - 1762
• Main Authors: Stenner, Max-Philipp, Bauer, Markus, Heinze, Hans-Jochen, Haggard, Patrick, Dolan, Raymond J.
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 15.03.2015
• Subjects: Adult; Anticipation, Psychological; Female; Functional Laterality; Hand - physiology; Humans; Male; Movement; Psychomotor Performance; Sensorimotor Cortex - physiology; Sensory Processing; sensory prediction; agency; motor priming; sensory attenuation; lateralized readiness potential
• ISSN: 0022-3077; 1522-1598; 1522-1598
• DOI: 10.1152/jn.00616.2014

Sensory consequences of one's own actions are perceived as less intense than identical, externally generated stimuli. This is generally taken as evidence for sensory prediction of action consequences. Accordingly, recent theoretical models explain this attenuation by an anticipatory modulation of sensory processing prior to stimulus onset (Roussel et al. 2013) or even action execution (Brown et al. 2013). Experimentally, prestimulus changes that occur in anticipation of self-generated sensations are difficult to disentangle from more general effects of stimulus expectation, attention and task load (performing an action). Here, we show that an established manipulation of subjective agency over a stimulus leads to a predictive modulation in sensory cortex that is independent of these factors. We recorded magnetoencephalography while subjects performed a simple action with either hand and judged the loudness of a tone caused by the action. Effector selection was manipulated by subliminal motor priming. Compatible priming is known to enhance a subjective experience of agency over a consequent stimulus (Chambon and Haggard 2012). In line with this effect on subjective agency, we found stronger sensory attenuation when the action that caused the tone was compatibly primed. This perceptual effect was reflected in a transient phase-locked signal in auditory cortex before stimulus onset and motor execution. Interestingly, this sensory signal emerged at a time when the hemispheric lateralization of motor signals in M1 indicated ongoing effector selection. Our findings confirm theoretical predictions of a sensory modulation prior to self-generated sensations and support the idea that a sensory prediction is generated in parallel to motor output (Walsh and Haggard 2010), before an efference copy becomes available.