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Every movement requires the nervous system to solve a complex biomechanical control problem, but this process is mostly veiled from one's conscious awareness. Simultaneously, we also have conscious experience of controlling our movements - our sense of agency (SoA). Whether SoA corresponds to those neural representations that implement actual neuromuscular control is an open question with ethical, medical, and legal implications. If SoA is the conscious experience of control, this predicts that SoA can be decoded from the same brain structures that implement the so-called inverse kinematic computations for planning movement. We correlated human fMRI measurements during hand movements with the internal representations of a deep neural network (DNN) performing the same hand control task in a biomechanical simulation - revealing detailed cortical encodings of sensorimotor states, idiosyncratic to each subject. We then manipulated SoA by usurping control of participants' muscles via electrical stimulation, and found that the same voxels which were best explained by modeled inverse kinematic representations - which, strikingly, were located in canonically visual areas - also predicted SoA. Importantly, model-brain correspondences and robust SoA decoding could both be achieved within single subjects, enabling relationships between motor representations and awareness to be studied at the level of the individual.
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Temporal Dynamics of Brain Activity Predicting Sense of Agency over Muscle Movements
Our muscles are the primary means through which we affect the external world, and the sense of agency (SoA) over the action through those muscles is fundamental to our self-awareness. However, SoA research to date has focused almost exclusively on agency over action outcomes rather than over the musculature itself, as it was believed that SoA over the musculature could not be manipulated directly. Drawing on methods from human–computer interaction and adaptive experimentation, we use human-in-the-loop Bayesian optimization to tune the timing of electrical muscle stimulation so as to robustly elicit a SoA over electrically actuated muscle movements in male and female human subjects. We use time-resolved decoding of subjects' EEG to estimate the time course of neural activity which predicts reported agency on a trial-by-trial basis. Like paradigms which assess SoA over action consequences, we found that the late (post-conscious) neural activity predicts SoA. Unlike typical paradigms, however, we also find patterns of early (sensorimotor) activity with distinct temporal dynamics predicts agency over muscle movements, suggesting that the “neural correlates of agency” may depend on the level of abstraction (i.e., direct sensorimotor feedback versus downstream consequences) most relevant to a given agency judgment. Moreover, fractal analysis of the EEG suggests that SoA-contingent dynamics of neural activity may modulate the sensitivity of the motor system to external input. SIGNIFICANCE STATEMENTThe sense of agency, the feeling of “I did that,” when directing one's own musculature is a core feature of human experience. We show that we can robustly manipulate the sense of agency over electrically actuated muscle movements, and we investigate the time course of neural activity that predicts the sense of agency over these actuated movements. We find evidence of two distinct neural processes: a transient sequence of patterns that begins in the early sensorineural response to muscle stimulation and a later, sustained signature of agency. These results shed light on the neural mechanisms by which we experience our movements as volitional.
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- Award ID(s):
- 2024923
- PAR ID:
- 10463628
- Publisher / Repository:
- DOI PREFIX: 10.1523
- Date Published:
- Journal Name:
- The Journal of Neuroscience
- Volume:
- 43
- Issue:
- 46
- ISSN:
- 0270-6474
- Format(s):
- Medium: X Size: p. 7842-7852
- Size(s):
- p. 7842-7852
- Sponsoring Org:
- National Science Foundation
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