Motor-evoked neural responses in auditory cortex are associated with improved sensitivity to self-generated sounds

Abstract

Sensory perception is a product of complex interactions between the internal state of an organism and the physical attributes of a stimulus. One factor that modulates the internal state of the perceiving agent is voluntary movement. It has been shown across the animal kingdom that perception and sensory-evoked physiological responses are modulated depending on whether or not the stimulus is the consequence of voluntary actions. These phenomena are often attributed to motor signals sent to relevant sensory regions (efference copies), that convey information about expected upcoming sensory consequences. However, to date, there is no direct evidence in humans for efferent signals underlying these motor-sensory interactions. In the current study we recorded neurophysiological (using Magnetoencephalography) and behavioral responses from 16 healthy subjects performing an auditory detection task of faint tones. Tones were either generated by subjects' voluntary button presses or occurred predictably following a visual cue.By introducing a constant temporal delay between button press/cue and tone delivery and applying source-level analysis we decoupled motor-evoked and auditory-evoked activity in auditory cortex. We show motor-related evoked-responses in auditory cortex following soundtriggering actions and preceding sound onset. Such evoked-responses were not found for buttonpresses that were not coupled with expected sounds. Furthermore, the amplitude of these evokedresponses corresponded with subsequent sound detection, suggesting their functional relevance to auditory processing. Our results provide first direct evidence for efferent signals in sensory cortex that are evoked by voluntary actions coupled with sensory consequences.

Memory-paced tapping to auditory rhythms: Effects of rate, speech and motor-engagement

“…There are also growing indications that motor movement can directly affect auditory perception, particularly when stimuli are rhythmic or temporally predictable (Thaut et al 2001; Schroeder et al 2010; Chemin et al 2014; Park et al 2015; Morillon and Baillet 2017; Rimmele et al 2018). Some examples for this are enhancement of perceptual thresholds (Reznik et al 2021), increased sensitivity to auditory pitch patterns (Lange 2009; Morillon et al 2014; Bauer et al 2015) and enhanced neural representations for rhythmic sounds following movement (Chemin et al 2014; Zalta et al 2020). The current finding that memory-paced tapping is significantly better after actively synchronizing to a reference rhythm vs. after hearing it passively provides yet another indication for the strong influence of motor action on auditory rhythm perception.…”

“…In other words, that accurate memory-paced tapping during the continuation phase is a product of cooperation between the auditory and motor systems during the synchronization phase. This perspective is motivated by the strong mutual influence observed between auditory perception and motor action, that manifests, for example, in perceptual enhancements brought about by movement (Thaut et al 2001; Schroeder et al 2010; Chemin et al 2014; Morillon et al 2014; Park et al 2015; Rimmele et al 2018; Gale et al 2021; Reznik et al 2021), as well as in the near automatic tendency to synchronize one’s body-movements to rhythmic sounds (Large 2008; Roerdink et al 2011; Repp and Su 2013; Tranchant et al 2016; Assaneo et al 2019; Damm et al 2020). Auditory-motor interactions are also hypothesized to involve neural oscillations as the backbone supporting communication and coupling between auditory and motor cortices and coordinating rhythmic behaviour (Arnal et al 2015; Breska and Deouell 2017; Morillon and Baillet 2017; Morillon et al 2019; Abbasi and Gross 2020).…”