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 (1-6s). 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 ones 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.