The generic inhibitory function of corollary discharge in motor intention: evidence from the modulation effects of speech preparation on the late components of auditory neural responses

Abstract

The importance of action-perception loops necessitates efficient computations linking motor and sensory systems. Corollary discharge (CD), a concept in motor-to-sensory transformation, has been proposed to predict the sensory consequences of actions for efficient motor and cognitive control. The predictive computation has been assumed to realize via inhibiting sensory reafference when actions are executed. Continuous control throughout the course of action demands inhibitory function ubiquitously on all potential reafference when sensory consequences are not available prior to execution. However, the temporal and functional characteristics of CD are unclear – When does CD begin to operate? To what extent does CD inhibit sensory processes? How is the inhibitory function implemented in neural computation? Using a delayed articulation paradigm with three types of auditory probes (speech, non-speech, and non-human sounds) in an electroencephalography (EEG) experiment with 20 human participants (7 male), we found that preparing to speak without knowing what to say (general preparation) suppressed neural responses to each type of auditory probe, suggesting a generic inhibitory function of CD in motor intention. Moreover, power and phase coherence in low-frequency bands (1-8 Hz) were both suppressed, indicating that inhibition was mediated by dampening response amplitude and adding temporal variance to sensory processes. Furthermore, inhibition was stronger for sounds that humans can produce than non-human sounds, hinting that the generic inhibitory function of CD is regulated by the established motor-sensory associations. These results suggest a functional and temporal granularity of corollary discharge that mediates multifaceted computations in motor and cognitive control.

Significance Statement

The feeling and actual control of one’s body are linked to the same phenomenon of sensorimotor interaction – sensory processes of self-induced stimuli are attenuated by a copy of motor signals, coined as corollary discharge (CD). However, when, to what extent, and how CD inhibits sensory processes remain unclear. Using a delayed articulation paradigm in an EEG experiment, we found that CD inhibited all speech, non-speech and non-human sounds even when participants intended to speak, with stronger inhibition of the sounds that humans can produce. The inhibition was mediated by dampening response amplitude and adding temporal variance in low-frequency neural responses to sensory stimuli. These results suggest functional granularity of CD throughout the course of actions for motor control.