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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

We asked which wiring measure predicts the preferred motion direction (PD) of each retinal ganglion cell (GC). We used the public e2198 data set: two-photon calcium responses to bars that moved in 8 directions and serial electron microscopy of the same mouse retina patch, with 47 GC types and human-verified matches for 326 GCs (Briggman et al. 2011; Bae et al. 2018). We compared two predictors with the calcium PD of 315 typed cells: the direction of starburst amacrine cell (SAC) dendrites that touch the GC, plus 180° (anti-parallel rule), and the soma-to-arbor direction, also from a disc that cannot reach the volume border. A registration of calcium regions to EM somata (median residual 0.91 µm) gave the image-to-EM map. We chose the remaining 90° step with the On-Off DS cells only, then kept the map fixed. For 26 tuned On-Off DS cells, the SAC rule gave a median absolute PD error of 12.3° (95% CI 8–15°; PD noise 2.5°). For 7 held-out transient On DS cells (7o), the error was 22.7° (12–38°), with a common +23° offset. The arbor direction did not predict PD in these types (median errors 60–144°). Sustained On DS cells had large SAC asymmetry but responded weakly to this fast bar. For the asymmetric Off types 2an and 2aw, both predictors pointed within 7–40° of the type PD, but neither predicted which cell had which PD (shuffle p ≥ 0.38). For 58 tuned cells of 25 other types, no predictor did better than random. Weak tuning of non-DS types shared one direction (234 cells, mean vector 0.115 toward 91°), and 2an and 2aw pointed 6–9° from it. The baseline before each bar correlated with the previous response (median r 0.31), and directions were shown in a fixed order. Thus this data set cannot show that arbor asymmetry causes 2an or 2aw tuning. Within types, SAC direction deviations did not consistently predict PD deviations; the type-mean SAC direction predicted as well as each cell's value. Across 37 types, SAC contact fraction followed DSI (Spearman 0.47). Limitations: one retina, one bar speed, contacts rather than synapses, and a shared tuning bias of unknown cause.

retina · direction selectivity · starburst amacrine cell · retinal ganglion cell · connectomics · electron microscopy · calcium imaging · structure-function · Eyewire · e2198 · dendritic asymmetry · J-RGC · mouse

Admitted 11 citing publications

References

6
  1. usesdoi:10.1016/j.cell.2018.04.040

    Source of the GC reconstructions, types, SAC contact counts, calcium-EM matches and code (e2198 Eyewire museum).

  2. supportsdoi:10.1038/nature09818

    Original e2198 data set and the anti-parallel SAC wiring rule; we extend it to all contacts, a held-out On DS type and per-cell errors with a fixed angle map.

  3. doi:10.1038/nature06739

    J-RGCs: asymmetric dendrites and ventral motion preference; motivates the arbor predictor.

  4. doi:10.1016/j.celrep.2016.04.069

    F-mini and F-midi asymmetric GC types (2an, 2aw, 63 in e2198).

  5. doi:10.1038/nature16468

    Functional GC types in mouse retina, including the transient On DS type that corresponds to 7o.

  6. doi:10.1038/nature22818

    DS cell preferred directions vary with retinal position; a possible source of within-type PD variation.

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