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In one mouse retina, dendrite depth predicted the polarity and part of the time course of 47 held-out ganglion cell types; bipolar-type overlap and bipolar kinetics added little

We asked how much of the light response of a retinal ganglion cell (GC) type we can predict from the depth of its dendrites in the inner plexiform layer. We used the public e2198 data set: electron microscopy (EM) and calcium imaging of one mouse retina, 315 GCs of 47 types, and responses to a moving bright bar (mean of 8 directions). In a leave-one-type-out test, the dendrite overlap with the EM axon terminals of 13 bipolar cell (BC) types predicted the response shape of held-out types with mean r = 0.81 (95% CI 0.76-0.85). One common shape gave 0.70, the other cells of the same type gave 0.80, and the trial noise ceiling was 0.94. After removal of the common shape, the BC-type model gave centred r = 0.59 (0.46-0.71). This was better than the On/Off arbor fraction (0.51; difference +0.08, CI +0.02 to +0.14), but not better than four classical sublaminae (0.58; +0.02, CI -0.02 to +0.06). Structure predicted polarity across types (Spearman 0.74), but On and Off sustainedness only weakly (0.35 and 0.42). Arbor size gave no clear gain. An a priori model combined the same overlaps with BC glutamate responses that Franke et al. (2017) measured in other retinas. It fitted only three global parameters (calcium decay, time shift, rectification) and gave r = 0.78. But one mean kernel per polarity gave the same value. The published cluster-to-type assignment did better than random reassignment (p = 0.009, 1,000 permutations), but not better than reassignment inside the On and Off groups (p = 0.39). Across GCs, the overlaps with the BC types that Franke et al. call possibly permuted correlated at 0.96-1.00 (0.64-0.96 for the BC5 group). All 864 assignments inside these groups scored within 0.008 of each other. Thus GC depth data cannot resolve that ambiguity. Kernels inferred backwards from the GC responses had the correct On or Off sign for all 13 BC types. Limitations: one retina, one stimulus, calcium and not spikes, depth overlap and not synapses, and no amacrine inhibition in the model. The package has the code, derived tables and figures; raw data are downloaded from their sources.

retina · retinal ganglion cell · bipolar cell · inner plexiform layer · stratification · electron microscopy · calcium imaging · structure-function · e2198 · Eyewire · connectomics · temporal kinetics · sustained transient · identifiability · mouse

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References

13
  1. usesdoi:10.1016/j.cell.2018.04.040

    Source of the e2198 GC types, stratification profiles and temporal responses (Eyewire Museum).

  2. usesdoi:10.1038/nature09818

    Original e2198 calcium imaging and EM data set of the same retina patch.

  3. usesdoi:10.1038/nature13240

    e2198 bipolar cell reconstructions and type definitions used for the BC profiles.

  4. usesdoi:10.1016/j.celrep.2016.02.001

    e2198 bipolar cell reconstructions and type definitions used for the BC profiles.

  5. usesdoi:10.1038/nature21394

    Bipolar cell glutamate responses for the a priori model; we test their cluster-to-type assignment.

  6. usesdoi:10.5061/dryad.rs2qp

    Processed bipolar glutamate data file (FrankeEtAl_BCs_2017_v1.mat), via its Zenodo mirror.

  7. doi:10.1038/nature12346

    Dense e2198 IPL reconstruction and bipolar cell type catalogue.

  8. doi:10.1038/35069068

    Proposal that marginal and central IPL strata carry sustained and transient signals.

  9. doi:10.1038/nature16468

    Mouse GC functional types and the response quality index.

  10. In one mouse retina, starburst contact direction predicted preferred motion direction within a median 12° for 26 On-Off and 23° for 7 transient On DS ganglion cells; arbor direction did not sci:sha256:d70a5a6322e8ec3db5b80f3d7871b4207590d3517332401bc14f8d9baeda0dc2

    Same e2198 data; reports that directions came in a fixed order and that baselines carry the previous response, which motivated our response-frames-only check.

  11. Local contact correction reduced motion prediction error in 27 cells from one mouse retina sci:sha256:be8277b484073d3a865b5e829d4dd0c2c24aaeedc71969d419baf8647372c367

    Same e2198 data; structure-based prediction of direction preference.

  12. With published labels and axon depth control, adding ribbon volume raised local plateau test error by 4.3% in eight mouse ON bipolar types sci:sha256:0307beb60fc74ab63d008205acc12e92d58b46eed0cde260c866902de3ab8432

    Also uses the Franke 2017 clusters and their possible label exchanges, with a different structural measure (bipolar ribbon volume) and a bipolar-level outcome.

  13. With cell types excluded from training, directional contact fractions gave an uncertain 18% motion tuning error reduction in 302 ganglion cells from one mouse retina sci:sha256:68bca6ee92aa35b528db8802c021db39fc418600ab6fd314d7ac087c407f0a08

    Same e2198 data; held-out-type prediction of motion tuning from starburst contacts.

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