Abstract
Voluntary action is a fundamental element of self-consciousness. The readiness potential (RP), a slow drift of neural activity preceding self-initiated movement, has been suggested to reflect neural processes underlying the preparation of voluntary action; yet more than fifty years after its introduction, interpretation of the RP remains controversial. Based on previous research showing that internal bodily signals affect sensory processing and ongoing neural activity, we here investigated the potential role of interoceptive signals in voluntary action and the RP. We report that (1) participants initiate voluntary actions more frequently during expiration, (2) this respiration-action coupling is absent during externally triggered actions, and (3) the RP amplitude is modulated depending on the respiratory phase. Our findings demonstrate that voluntary action is coupled with the respiratory system and further suggest that the RP is associated with fluctuations of ongoing neural activity that are driven by the involuntary and cyclic motor act of breathing.
Highlights
Voluntary action is a fundamental element of self-consciousness
This decade-long interpretation has been challenged, with Schurger and colleagues proposing that the readiness potential (RP) reflects spontaneous fluctuation of background neuronal activity or noise, rather than a specific neural process underlying the preparation of voluntary action[7,8,9]
We show that fluctuations of respiratory, but not cardiac, phase are coupled with the onset of voluntary action and the neural hallmark of voluntary action, the RP, and further that such respiration-action coupling is absent during externally triggered actions
Summary
Voluntary action is a fundamental element of self-consciousness. The readiness potential (RP), a slow drift of neural activity preceding self-initiated movement, has been suggested to reflect neural processes underlying the preparation of voluntary action; yet more than fifty years after its introduction, interpretation of the RP remains controversial. Together with Libet’s seminal observation that the onset of the RP precedes participants’ conscious intention of a movement[5], the RP has been interpreted as an unconscious cortical precursor to conscious intention[6] This decade-long interpretation has been challenged, with Schurger and colleagues proposing that the RP reflects spontaneous fluctuation of background neuronal activity or noise, rather than a specific neural process underlying the preparation of voluntary action[7,8,9]. Few studies have measured respiration signals during voluntary movement tasks, it has rather been considered as physiological noise[20] Based on these three lines of evidence, we predicted that interoceptive signals, in particular respiration, could be the source of the apparently spontaneous fluctuations of background neuronal activity that has been linked to the RP8. We show that fluctuations of respiratory, but not cardiac, phase are coupled with the onset of voluntary action and the neural hallmark of voluntary action, the RP, and further that such respiration-action coupling is absent during externally triggered actions
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