Modeling semantic encoding in a common neural representational space

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Abstract

Encoding models for mapping voxelwise semantic tuning are typically estimated separately for each individual, limiting their generalizability. In the current report, we develop a method for estimating semantic encoding models that generalize across individuals. Functional MRI was used to measure brain responses while participants freely viewed a naturalistic audiovisual movie. Word embeddings capturing agent-, action-, object-, and scene-related semantic content were assigned to each imaging volume based on an annotation of the film. We constructed both conventional within-subject semantic encoding models and between-subject models where the model was trained on a subset of participants and validated on a left-out participant. Between-subject models were trained using cortical surface-based anatomical normalization or surface-based whole-cortex hyperalignment. We used hyperalignment to project group data into an individual's unique anatomical space via a common representational space, thus leveraging a larger volume of data for out-of-sample prediction while preserving the individual's fine-grained functional-anatomical idiosyncrasies. Our findings demonstrate that anatomical normalization degrades the spatial specificity of between-subject encoding models relative to within-subject models. Hyperalignment, on the other hand, recovers the spatial specificity of semantic tuning lost during anatomical normalization, and yields model performance exceeding that of within-subject models.

Figures

  • FIGURE 1 | Schematic for constructing between-subject semantic encoding models using hyperalignment. The schematic depicts onefold of the nested leave-one-out cross-validation procedure repeated for 4 test runs and 18 test participants (72 cross-validation folds in total). (A) Training between-subject semantic encoding models using ridge regression. Regression coefficients (weights) are estimated to predict response time series per vertex based on three training runs. (B) Testing semantic encoding models. Regression weights estimated on training data are used to predict response time series for a fourth test run. Model prediction performance is evaluated by computing the Pearson correlation between the predicted responses and are the actual response time series per vertex. (C) Hyperalignment for between-subject semantic encoding models. For each test subject in the leave-one-subject-out cross-validation procedure, we first projected each training subject’s data into the common space using their subject-specific hyperalignment transformations. We then use the transpose of the test subject’s hyperalignment transformation to project all training subjects’ data into the test subject’s space. We averaged response vectors for all training subjects in the test subject’s space, then trained the encoding model on this averaged response trajectory. Finally, we evaluated between-subject model performance by predicting vertex-wise response time series for the left-out test run in the left-out test participant, and computed the Pearson correlation between the predicted time series and the actual time series per vertex.
  • FIGURE 2 | Hyperalignment improves inter-subject correlation (ISC) of response profiles and representational geometry. (A) ISC of vertex-wise response time series before and after hyperalignment. Colored vertices reflect the mean ISC across subjects, thresholded at a mean correlation of 0.2. ISCs are highest in the superior temporal gyrus (in the vicinity of auditory cortex), as well as the dorsal and ventral visual pathways, comprising early visual, lateral occipitotemporal, ventral temporal, posterior parietal, and intraparietal cortices. (B) ISC of searchlight representational geometries (time-point RDMs in 9 mm radius searchlights) before and after hyperalignment. Colored vertices reflect the mean pairwise correlation across subjects for each searchlight, thresholded at a mean correlation of 0.2, revealing a broader extent of cortex with improved alignment of functional topography after hyperalignment. ISCs were Fisher z-transformed before averaging across all subjects and inverse Fisher transformed before mapping onto the cortical surface for visualization. All maps are rendered on the fsaverage6 surface template.
  • FIGURE 3 | Model prediction performance maps for two example subjects (left and right). Colored vertices reflect the Pearson correlation between the predicted and actual time series averaged across the four test runs. Three types of models are presented: (A) within-subject model performance maps; (B) between-subject anatomically aligned model performance maps; and (C) between-subject hyperaligned model performance maps. Maximum correlations are 0.37 (both subjects 12 and 14, area LO, all three maps) and correlations at the 95% level for vertices within the mask ranged from 0.29 to 0.31. All maps are unthresholded and uncorrected for multiple tests.
  • FIGURE 4 | Model prediction performance maps averaged across subjects. Colored vertices reflect the Pearson correlation between the predicted and actual time series averaged across the four test runs and averaged across subjects. Three types of models are presented: (A) within-subject model performance maps; (B) between-subject anatomically aligned model performance maps; and (C) between-subject hyperaligned model performance maps. Maximum correlations are 0.27 (in area LO, all three maps) and correlations at the 95% level for vertices within the mask ranged from 0.11 to 0.12. All maps are unthresholded and uncorrected for multiple tests.
  • FIGURE 5 | Differences in semantic encoding model performance maps. (A) Paired differences in model performance between between-subject models using anatomical normalization and within-subject models. Warm colors indicate vertices where the anatomically aligned between-subject model performance exceeds within-subject model performance, and cool colors indicate where within-subject model performance exceeds anatomically aligned between-subject model performance. (B) Paired differences in model performance between between-subject models using hyperalignment and within-subject models. Warm colors indicate vertices where the hyperaligned between-subject model performance exceeds within-subject model performance, and cool colors indicate where within-subject model performance exceeds hyperaligned between-subject model performance. (C) Paired differences in model performance for between-subject models using hyperalignment and anatomical normalization. Warm colors indicate vertices where the hyperaligned between-subject model performance exceeds anatomically aligned between-subject model performance, and cool colors indicate where anatomically aligned between-subject model performance exceeds hyperaligned between-subject model performance. Colored vertices reflect mean paired differences in model performance, thresholded at an absolute t-value of t(17) = 2.11, p < 0.05, uncorrected for multiple comparisons.
  • FIGURE 6 | Spatial PSF of semantic tuning. (A) Correlation between the predicted time series of one vertex and the actual time-series of its neighboring vertices up to 12 mm away. Correlations were aggregated based on distance from the central vertex of interest and averaged across vertices and subjects. Error bars denote 68% confidence intervals (standard error of the mean). (B) The within-subject and hyperaligned between-subject models have the steepest slopes (negative of the slope based on logarithmic curve fitting). Error bars denote 95% confidence intervals obtained by bootstrapping subjects 20,000 times with replacement.
  • FIGURE 7 | Spatial smoothness (FWHM) of model prediction performance maps on the cortical surface. The between-subject model performance maps using anatomical alignment are blurred relative to the within-subject model performance maps, while the hyperaligned between-subject model recovers the spatial specificity of the within-subject model. The height of each bar indicates spatial smoothness averaged across hemispheres and participants for each run. Error bars indicate bootstrapped 95% confidence intervals estimated by resampling participants (1,000 bootstrap samples).
  • FIGURE 8 | Spatial correlation between within-subject model prediction performance maps and between-subject model prediction performance maps using either anatomical alignment or hyperalignment. The between-subject model using hyperalignment yielded a model performance map that is more similar to the within-subject model than the model performance map of the between-subject model using anatomical alignment. The height of each bar indicates mean spatial correlation across participants for each run. Error bars indicate bootstrapped 95% confidence intervals estimated by resampling participants (1,000 bootstrap samples).

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CITATION STYLE

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Van Uden, C. E., Nastase, S. A., Connolly, A. C., Feilong, M., Hansen, I., Ida Gobbini, M., & Haxby, J. V. (2018). Modeling semantic encoding in a common neural representational space. Frontiers in Neuroscience, 12(JUL). https://doi.org/10.3389/fnins.2018.00437

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