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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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Neuroimaging Signatures of Metacognitive Improvement in Sensorimotor Timing
Error monitoring is an essential human ability underlying learning and metacognition. In the time domain, humans possess a remarkable ability to learn and adapt to temporal intervals, yet the neural mechanisms underlying this are not well understood. Recently, we demonstrated that humans exhibit improvements in sensorimotor time estimates when given the chance to incorporate feedback from a previous trial (Bader and Wiener, 2021), suggesting that humans are metacognitively aware of their own timing errors. To test the neural basis of this metacognitive ability, human participants of both sexes underwent fMRI while they performed a visual temporal reproduction task with randomized suprasecond intervals (1.5-6s). Crucially, each trial was repeated following feedback, allowing a “re-do” to learn from the successes or errors in the initial trial. Behaviorally, we replicated our previous finding that subjects improve their performance on re-do trials despite the feedback being temporally uninformative (i.e. early or late). For neuroimaging, we observed a dissociation between estimating and reproducing time intervals, with the former more likely to engage regions associated with the default mode network (DMN), including the superior frontal gyri, precuneus, and posterior cingulate, whereas the latter activated regions associated traditionally with the “Timing Network” (TN), including the supplementary motor area (SMA), precentral gyrus, and right supramarginal gyrus. Notably, greater DMN involvement was observed in Re-do trials. Further, the extent of the DMN was greater on re-do trials, whereas for the TN it was more constrained. Finally, Task-based connectivity between these networks demonstrated higher inter-network correlation on initial trials, but primarily when estimating trials, whereas on re-do trials communication was higher during reproduction. Overall, these results suggest the DMN and TN work in concert to mediate subjective awareness of one’s sense of time for the purpose of improving timing performance. Significance StatementA finely tuned sense of time perception is imperative for everyday motor actions (e.g., hitting a baseball). Timing self-regulation requires correct assessment and updating duration estimates if necessary. Using a modified version of a classical task of time measurement, we explored the neural regions involved in error detection, time awareness, and learning to time. Reinforcing the role of the SMA in measuring temporal information and providing evidence of co-activation with the DMN, this study demonstrates that the brain overlays sensorimotor timing with a metacognitive awareness of its passage.
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- Award ID(s):
- 1922598
- PAR ID:
- 10541571
- Publisher / Repository:
- Society for Neuroscience
- Date Published:
- Journal Name:
- The Journal of Neuroscience
- ISSN:
- 0270-6474
- Page Range / eLocation ID:
- JN-RM-1789-22
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1523/JNEUROSCI.1789-22.2023
