Neuroimaging Signatures of Metacognitive Improvement in Sensorimotor Timing

J Neurosci. 2024 Feb 28;44(9):e1789222023. doi: 10.1523/JNEUROSCI.1789-22.2023.

Abstract

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 clear. Recently, we demonstrated that humans improve sensorimotor time estimates when given the chance to incorporate previous trial feedback ( 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 supra-second intervals (1.5-6 s). 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 of improved re-do trial performance despite temporally uninformative (i.e., early or late) feedback. For neuroimaging, we observed a dissociation between estimating and reproducing time intervals. Estimation engaged the default mode network (DMN), including the superior frontal gyri, precuneus, and posterior cingulate, whereas reproduction activated regions associated traditionally with the "timing network" (TN), including the supplementary motor area (SMA), precentral gyrus, and right supramarginal gyrus. Notably, greater and more extensive DMN involvement was observed in re-do trials, whereas for the TN, it was more constrained. Task-based connectivity between these networks demonstrated higher inter-network correlation primarily when estimating initial trials, while re-do trial communication was higher during reproduction. Overall, these results suggest that the DMN and TN jointly mediate subjective self-awareness to improve timing performance.

MeSH terms

  • Brain Mapping / methods
  • Brain* / diagnostic imaging
  • Female
  • Humans
  • Magnetic Resonance Imaging / methods
  • Male
  • Metacognition*
  • Neuroimaging