Hunt JE et al. (2024), OCULAR NECESSITIES: A NEUROETHOLOGICAL PERSPECT...

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Brain Behav Evol 2024 Mar 06; doi: 10.1159/000536035.

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OCULAR NECESSITIES: A NEUROETHOLOGICAL PERSPECTIVE ON VERTEBRATE VISUAL DEVELOPMENT.

Hunt JE , Pratt KG , Molnar Z .

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BACKGROUND: By examining species-specific innate behaviours, neuroethologists have characterised unique neural strategies and specializations from throughout the animal kingdom. Simultaneously, the field of evolutionary developmental biology (informally, "evo-devo") seeks to make inferences about animals' evolutionary histories through careful comparison of developmental processes between species, because evolution is the evolution of development. Yet despite the shared focus on cross-species comparisons, there is surprisingly little cross-talk between these two fields. Insights can be gleaned at the intersection of neuroethology and evo-devo. Every animal develops within an environment, wherein ecological pressures advantage some behaviours and disadvantage others. These pressures are reflected in the neurodevelopmental strategies employed by different animals across taxa. SUMMARY: Vision is a system of particular interest for studying the adaptation of animals to their environments. The visual system enables a wide variety of animals across the vertebrate lineage to interact with their environments, presenting a fantastic opportunity to examine how ecological pressures have shaped animals' behaviours and developmental strategies. Applying a neuroethological lens to the study of visual development, we advance a novel theory that accounts for the evolution of spontaneous retinal waves, an important phenomenon in the development of the visual system, across the vertebrate lineage. KEY MESSAGES: We synthesise literature on spontaneous retinal waves from across the vertebrate lineage. We find that ethological considerations explain some cross-species differences in the dynamics of retinal waves. In zebrafish, retinal waves may be more important for the development of the retina itself, rather than the retinofugal projections. We additionally suggest empirical tests to determine whether Xenopus laevis experiences retinal waves.

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	Fig. 1. Cladogram depicting the study of spontaneous retinal waves across species. A green silhouette and check indicates retinal waves have been observed in this phylogenetic group. A red silhouette and cross indicates that observations have failed to detect retinal waves in this group. To our knowledge, retinal waves have not been studied in any taxonomic group besides those indicated here.
	Fig. 2. Temporal-to-nasal patterned retinal activity – whether spontaneous or evoked by light. a Spontaneous retinal waves stereotypically propagate from the temporal side of the retina to the nasal side. b As a tadpole swims forward, the visual scene stimulates the retina in the same temporal-to-nasal manner. c Similarly, the visual environment stimulates the mouse’s retina temporally-to-nasally as the mouse runs forward. Figure produced by Mr. Erick Fernandez de Arteaga.
	Fig. 3. Development of the Xenopus visual system. a At stage 35–37, approximately 2 days post-fertilization, the IPL first forms. At this time, bipolar cells begin to synapse onto RGCs. It is unknown whether retinal waves occur in any layer at this stage. Schematic shows the organization of the Xenopus retina, including the IPL. b At stage 39–40, approximately 2.5–3 days post-fertilization, synaptogenesis continues in the IPL. The first retinofugal synapses begin to form between RGCs and tectal cells. Retinal waves do not occur in the RGC layer, per experiments reported by Demas et al. [21]. Xenopus illustrations, stage 37–38 (a) and 40 (b) © Natalya Zahn (2022) [53], via Xenbase (www.xenbase.org RRID:SCR_003280). Scale bars: 1 mm.

References [+] :

Ackman, Retinal waves coordinate patterned activity throughout the developing visual system. 2012, Pubmed