Double cones in the avian retina form an oriented mosaic which might facilitate magnetoreception and/or polarized light sensing

Abstract

To navigate between breeding and wintering grounds, night-migratory songbirds are aided by a light-dependent magnetic compass sense and maybe also by polarized light vision. Although the underlying mechanisms for magnetoreception and polarized light sensing remain unclear, double cone photoreceptors in the avian retina have been suggested to represent the primary sensory cells. To use these senses, birds must be able to separate the directional information from the Earth's magnetic field and/or light polarization from variations in light intensity. Theoretical considerations suggest that this could be best achieved if neighbouring double cones were oriented in an ordered pattern. Therefore, we investigate the orientation patterns of double cones in European robins ( Erithacus rubecula ) and domestic chickens ( Gallus gallus domesticus ). We used whole-mounted retinas labelled with double cone markers to quantify the orientations of individual double cones in relation to their nearest neighbours. In both species, our data show that the double cone array is highly ordered: the angles between neighbouring double cones were more likely to be 90°/−90° in the central retina and 180°/0° in the peripheral retina, respectively. The observed regularity in double cone orientation could aid the cells' putative function in light-dependent magnetoreception and/or polarized light sensing.

Isotope Substitution Effects on the Magnetic Compass Properties of Cryptochrome-Based Radical Pairs: A Computational Study

“…A smaller reduction in ΔΦ S (compared to the unsubstituted case) is seen when any two of C4, C4a, and C8α are substituted (bars 5−7 in Figure 4a). Replacing a fourth 12 C by 13 C, in addition to C4, C4a, and C8α, gave neither a further reduction in ΔΦ S (Figure 4e) nor much of a change in the θdependence (Figure 4g).…”

“…In the context of magnetoreception, the relevant quantities are the variation of the reaction yield, Φ S (θ, ϕ), with the direction of a ∼50 μT magnetic field and the magnitude of this anisotropy, ΔΦ S (eq 1). In the calculations reported here, we explored the effects of replacing 1 H by 2 H, 12 C by 13 C, and 14 N by 15 N, for both of the candidate radical pairs in cryptochrome: FAD-Trp and FAD-Z. Broadly similar magnetic isotope effects were found for FAD-Trp and FAD-Z, with FAD-Z having ΔΦ S values about twice those of FAD-Trp, other things being equal (Figures 2−4).…”

“…Migratory songbirds have a remarkable ability to use the direction of the Earth’s magnetic field to help them navigate between their breeding and wintering grounds. , The biophysical mechanism of this light-dependent magnetic compass is uncertain but seems to involve magnetically sensitive photochemical reactions within photoreceptor cells in the retina. − The most likely magnetoreceptor is Cry4a, one of the six known avian cryptochrome (Cry) proteins, in which short-lived radical pairs can be formed by the passage of an electron along a chain of four tryptophan (TrpH) residues to the photoexcited flavin adenine dinucleotide (FAD) chromophore in the center of the protein. ,− In support of this proposal, flavin-tryptophan radical pairs, [FAD •– TrpH •+ ], in purified Cry4a from the migratory European robin ( Erithacus rubecula , Er ) have recently been shown to be sensitive to weak applied magnetic fields. , However, it has yet to be demonstrated that Cry4a has the same photochemistry in vivo or that it satisfies other requirements for a viable magnetic direction sensor. Another possibility, for which there is currently less evidence, is that the magnetic sensitivity in vivo originates in a different radical pair, formed during the dark recovery of a photochemically reduced state of the protein. − There has also been some discussion of Cry1a as an alternative to Cry4a, even though it does not bind FAD strongly in vitro . − …”

Immunohistochemical characterization of bipolar cells in four distantly related avian species

“…Photoreceptor connections of selected bipolar cell types in the European robin retina Photoreceptors may be the initiation point for magnetoreception in night-migratory songbirds. As the best supported sensory molecule, cryptochrome 4 (Xu et al, 2021), is expressed in the outer and inner segments of double cones and long-wavelength single cones in the European robin retina (Chetverikova et al, 2022;Günther et al, 2018), we were also interested in finding bipolar cells that contact these photoreceptors because they may carry magnetic signals in addition to visual signals. However, only three bipolar cell markers were suitable for assessing the photoreceptor connections.…”

“…One of the four species, the European robin, is also well known for its ability to orient with the help of the Earth's magnetic field (Mouritsen, 2018; Wiltschko & Wiltschko, 1972; Zapka et al., 2009) during nighttime migration. This ability is based on a light‐dependent process (Hore & Mouritsen, 2016; Ritz et al., 2000; Xu et al., 2021), which seems to start in the retina (Heyers et al., 2007; Liedvogel et al., 2007; Mouritsen et al., 2005), namely in the double cone photoreceptors (Chetverikova et al., 2022; Günther et al., 2018). To gain more insights into the retinal downstream circuitry that might be involved in magnetoreception, we also studied the photoreceptor connectivity of selected bipolar cell types in the European robin retina.…”