Mesoscale cortex-wide neural dynamics predict self-initiated actions in mice several seconds prior to movement

Abstract

ABSTRACTVolition - the sense of control or agency over one’s voluntary actions - is widely recognized as the basis of both human subjective experience and natural behavior in non-human animals. To date, several human studies have found peaks in neural activity preceding voluntary actions, e.g. the readiness potential (RP), and some have shown upcoming actions could be decoded even before awareness. While these findings may pose a challenge to traditional accounts of human volition, some have proposed that random processes underlie and explain pre-movement neural activity. Here we seek to address part of this controversy by evaluating whether pre-movement neural activity in mice contains structure beyond that present in random neural activity. Implementing a self-initiated water-rewarded lever pull paradigm in mice while recording widefield [Ca++] neural activity we find that cortical activity changes in variance seconds prior to movement and that upcoming lever pulls or spontaneous body movements could be predicted between 1 second to more than 10 seconds prior to movement, similar to but even earlier than in human studies. We show that mice, like humans, are biased towards initiation of voluntary actions during specific phases of neural activity oscillations but that the pre-movement neural code in mice changes over time and is widely distributed as behavior prediction improved when using all vs single cortical areas. These findings support the presence of structured multi-second neural dynamics preceding voluntary action beyond that expected from random processes. Our results also suggest that neural mechanisms underlying self-initiated voluntary action could be preserved between mice and humans.