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A retinotopic code structures the interaction between perception and memory systems

Nature Neuroscience volume 27, pages 339–347 (2024)Cite this article

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Abstract

Conventional views of brain organization suggest that regions at the top of the cortical hierarchy processes internally oriented information using an abstract amodal neural code. Despite this, recent reports have described the presence of retinotopic coding at the cortical apex, including the default mode network. What is the functional role of retinotopic coding atop the cortical hierarchy? Here we report that retinotopic coding structures interactions between internally oriented (mnemonic) and externally oriented (perceptual) brain areas. Using functional magnetic resonance imaging, we observed robust inverted (negative) retinotopic coding in category-selective memory areas at the cortical apex, which is functionally linked to the classic (positive) retinotopic coding in category-selective perceptual areas in high-level visual cortex. These functionally linked retinotopic populations in mnemonic and perceptual areas exhibit spatially specific opponent responses during both bottom-up perception and top-down recall, suggesting that these areas are interlocked in a mutually inhibitory dynamic. These results show that retinotopic coding structures interactions between perceptual and mnemonic neural systems, providing a scaffold for their dynamic interaction.

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Fig. 1: pRF mapping reveals retinotopic coding throughout the posterior cortex, comprised of both positive- and negative-amplitude pRFs.
Fig. 2: Transition to mnemonic cortex is marked by the appearance of negative pRFs.
Fig. 3: Memory areas contain smaller pRFs compared to their paired perceptual areas.
Fig. 4: Shared visual-field representations between paired perception and memory areas.
Fig. 5: Positive pRFs in SPAs and negative pRFs in PMAs exhibit a spatially specific push–pull dynamic during memory recall.
Fig. 6: Positive pRFs in SPAs and negative pRFs in PMAs exhibit a push–pull dynamic during perception of familiar scene images.

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Data availability

Data are available on Open Science Framework (https://osf.io/sm2xf).

Code availability

Code used for data analysis is available on Open Science Framework (https://osf.io/sm2xf).

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Acknowledgements

We thank I. Groen for assistance with specific analysis code. This work was supported by the National Institute of Mental Health under award number R01MH130529 (C.E.R.). A.S. was supported by the Neukom Institute for Computational Science and E.H.S. by the Biotechnology and Biological Sciences Research Council award number BB/V003917/1.

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  1. These authors contributed equally: Adam Steel, Edward H. Silson.

Authors and Affiliations

  1. Department of Psychology and Brain Sciences, Dartmouth College, Hanover, NH, USA

    Adam Steel, Brenda D. Garcia & Caroline E. Robertson

  2. Psychosophy, Psychology, and Language Sciences, University of Edinburgh, Edinburgh, UK

    Edward H. Silson

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Contributions

A.S., E.H.S. and C.E.R. conceived of and designed the experiment. E.H.S. and B.D.G. contributed stimulus code. A.S. and B.D.G. collected the data. A.S. processed the data. A.S. and E.H.S. analyzed the data. A.S., E.H.S. and C.E.R. wrote and edited the paper.

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Correspondence to Adam Steel or Caroline E. Robertson.

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Extended data

Extended Data Fig. 1 Transition from positive to negative-amplitude population receptive fields (+pRF, -pRF) moving anteriorly from posterior cerebral cortex is evident in individual participants.

Figure depicts amplitude maps from all participants’ left hemispheres. Only vertices surviving the threshold applied in the main text (R2 > 0.08) are shown. Individual participant SPAs and PMAs used for analysis are drawn in white (PMAs) and black (SPAs).

Extended Data Fig. 2 Retinotopic coding in SPAs and PMAs.

To quantify the extent to which retinotopic coding is expressed within each ROI we first calculated the percentage of suprathreshold pRFs (R2 > 0.08) within our ROIs for each subject separately before testing each against a non-retinotopic prediction using t-tests (that is, t-test versus zero, with Bonferroni correction). Retinotopic coding was significantly present within each ROI (LH; OPA: t(12.51)=, pcorr = 3.35-9, D = 2.99; PPA: t(16) = 8.68, pcorr = 5.67-7, D = 2.17; LPMA: t(16) = 6.23, pcorr = 3.58-5, D = 1.59; VPMA: t(16) = 6.65, pcorr = 1.64-5, D = 1.66; RH; OPA: t(16) = 12.15, pcorr = 5.10-9, D = 3.03; PPA: t(16) = 11.97, pcorr = 6.32-9, D = 3.12; LPMA: t(16) = 8.75, pcorr = 5.05-7, D = 2.18; VPMA: t(16) = 6.39, pcorr = 2.68-5, D = 1.55). Bars represent the mean percentage of suprathreshold pRFs (R2 > 0.08) in each ROI/hemisphere for the lateral (left) and ventral (right) surfaces, respectively. Individual data points are overlaid. Each ROI exhibited a significant percentage of suprathreshold pRFs, ***ptwo-tailed < 0.001.

Extended Data Fig. 3 Comparison between the location of the SPAs, PMAs, and default mode network in one participant.

Comparison between the location of the SPAs, PMAs, and default mode network in one participant (example participant from Main text Fig. 2). This pattern was consistent in all individuals and at the group-level (Main text Fig. 1b). Default mode network defined using the Yeo et al., 2011 parcellation24.

Extended Data Fig. 4 Correlation in trial × trial activation during memory recall aggregated across participants.

Mean BOLD response amplitude relative to baseline during place recall trials for each ROI (OPA, LMPA) and pRF population (+/−).

Extended Data Fig. 5 Differential interaction between pRFs in SPAs with −/+ pRFs in memory areas is evident across all trials.

Each scatter plot and corresponding correlation values depict the unique correlation between pRFs in the SPAs with -pRFs (blue) and +pRFs (red) in the PMAs (for example, correlation between +pRFs in OPA with -pRFs in LPMA, controlling for +pRFs in LPMA) quantified using Pearson’s correlation. Each data point represents the z-scored activation on a given trial for all pRFS in the population (that is, all -LPMA pRFS) for a given subject on a trial.

Extended Data Fig. 6 Trial x trial interaction between −/+ pRFs in the place memory areas and scene perception areas exhibit push-pull interaction in independent data.

Recall trials were identical to the trials used in the localizer. Participants fixated on a dot projected in the center of the screen. They were then cued with the stimulus to be recalled for 1 second, followed by a 1 s dynamic mask, and 10 seconds of imagery. Trials were separated by a 4-8 s jittered interstimulus interval. Participants completed 32 imagery trials (16 for each landmark) separated into two imaging runs. One participant was excluded from the analysis for lack of familiarity with the landmarks; the remaining participants were familiar with the locations and had lived in the Hanover area for at least one year. Two participants did not have -pRFs in the ventral surface regions of interest. We tested for the relationship between +/− pRFs in the scene perception and place memory area using the same approach described in the Main text. We examined the unique correlation between the -/+ pRFs in the place memory areas and scene perception areas (that is, correlation between activation of -pRFs in memory areas with pRFs in scene perception areas, while controlling for activation of +pRFs in the memory areas). Using paired t-tests, we found evidence for the opponent interaction between -pRFs and +pRFs in this independent sample. We found that the relationship between the -/+ pRFs in the memory areas with the scene perception area pRFs was significantly different (Lateral – t(8) = 2.61, p = 0.018; Ventral – t(6) = 7.82, p < 0.0001). As we observed in our original analysis, the majority of participants showed a negative correlation in the trial x trial activation of the -pRFs in the place memory areas with pRFs in the scene perception areas (Ventral – 6/7 participants: t(6) = 2.79, p = 0.031; Lateral – 6/8 participants: t(8) = 1.79, p = 0.11). Likewise, most participants showed a positive relationship between activation of + pRFs in the memory areas and pRFs in the perception areas (Ventral – 7/7 participants; t(6) = 7.77, p = 0.0002; Lateral – 7/8 participants; t(8) = 3.30, p = 0.01). This result gives us confidence that our original analysis was not influenced by potential circularity. * = ptwo-tailed < 0.05, *** = ptwo-tailed < 0.005.

Extended Data Fig. 7 Activation during recall of personally familiar places.

Mean BOLD response amplitude relative to baseline when familiar scenes were presented in each lower quadrant (hemifield: ipsilateral and contralateral) for each ROI (OPA, LPMA) and pRF population (+/−).

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Steel, A., Silson, E.H., Garcia, B.D. et al. A retinotopic code structures the interaction between perception and memory systems. Nat Neurosci 27, 339–347 (2024). https://doi.org/10.1038/s41593-023-01512-3

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