Abstract
Humans automatically infer higher-order relationships between events in the environment from their statistical co-occurrence, often without conscious awareness. Neural replay of task representations is a candidate mechanism by which the brain learns such relational information or samples from a learned model in the service of adaptive behavior. Here, we tested whether cortical reactivation is related to learning higher-order sequential relationships without consciousness. Human participants viewed sequences of images that followed probabilistic transitions determined by ring-like graph structures. Behavioral modeling revealed that participants acquired multi-step transition knowledge through gradual updating of an internal successor representation (SR) model, although half of participants did not indicate conscious knowledge about the sequential task structure. To investigate neural replay, we analyzed the temporal dynamics of multivariate functional magnetic resonance imaging (fMRI) patterns during brief 10 seconds pauses from the ongoing statistical learning task. We found evidence for backward sequential replay of multi-step sequences in visual cortical areas. These findings indicate that implicit learning of higher-order relationships establishes an internal SR-based map of the task, and is accompanied by cortical on-task replay.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
The manuscript has been substantially revised. Major updates include: (1) We have added participant-specific fitting of successor representation (SR) models, which confirmed our previous finding that participants learn multi-step transition knowledge in an incidental sequence learning task. (2) We extended our modeling approach to capture the temporal dynamics of multivariate classifier time courses, allowing us to account for stimulus-driven activation patterns in on-task intervals and distinguish them from putative replay-driven (re)activation patterns. (3) We found evidence for backward sequential replay of multi-step (SR) sequences in visual cortical areas after accounting for stimulus-driven activity. (4) We investigated the influence of conscious task knowledge on SR learning and SR relay and found both to be independent of consciousness. (5) Finally, we found a correlation between the depth of the SR predictive horizon (gamma parameter) and the strength of SR replay during on-task intervals.
Glossary
- AC-PC
- anterior commissure - posterior commissure.
- AIC
- Akaike information criterion.
- ANOVA
- analysis of variance.
- ANTs
- Advanced Normalization Tools.
- A-P
- anterior-to-posterior.
- BIDS
- brain imaging data structure.
- BOBYQA
- Bound Optimization BY Quadratic Approximation.
- BOLD
- blood-oxygen-level dependent.
- CI
- confidence interval.
- COBYLA
- Constrained Optimization BY Linear Approximations.
- CSF
- cerebrospinal fluid.
- DGPs
- German Psychological Society.
- DICOM
- Digital Imaging and Communications in Medicine.
- EPI
- echo-planar imaging.
- FA
- flip angle.
- FD
- framewise displacement.
- FDR
- false discovery rate.
- fMRI
- functional magnetic resonance imaging.
- FOV
- field of view.
- FSL
- FMRIB Software Library.
- FWHM
- Full Width at Half Maximum.
- GLM
- general linear model.
- GM
- gray-matter.
- GR
- gradient recalled.
- HPC
- high performance computing.
- HRF
- The hemodynamic response function (HRF) characterizes an fMRI response that results from a brief, spatially localized pulse of neuronal activity.
- HSD
- honest significant difference.
- INU
- intensity non-uniformity.
- IQR
- interquartile range.
- ITI
- inter-trial interval.
- LME
- linear mixed effects.
- LTS
- long-term support.
- MB
- multi-band.
- min
- minute.
- MPRAGE
- Magnetization Prepared Rapid Gradient Echo.
- MRI
- magnetic resonance imaging.
- ms
- millisecond.
- PFC
- prefrontal cortex.
- PMU
- Physiological Measurement Unit.
- ROI
- region of interest.
- s
- second.
- SD
- standard deviation.
- SEM
- standard error of the mean.
- SI
- supplementary information.
- SR
- successor representation.
- S-R
- stimulus-response.
- SRI
- stimulus-response interval.
- SSE
- sum of squared errors.
- SUSAN
- Smallest Univalue Segment Assimilating Nucleus.
- T1w
- T1-weighted.
- TD
- temporal difference.
- TE
- echo time.
- TI
- inversion time.
- TR
- repetition time.
- WM
- white-matter.
