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From the eye to the wing: neural circuits for transforming optic flow into motor output in avian flight

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Abstract

Avian flight is guided by optic flow—the movement across the retina of images of surfaces and edges in the environment due to self-motion. In all vertebrates, there is a short pathway for optic flow information to reach pre-motor areas: retinal-recipient regions in the midbrain encode optic flow, which is then sent to the cerebellum. One well-known role for optic flow pathways to the cerebellum is the control of stabilizing eye movements (the optokinetic response). However, the role of this pathway in controlling locomotion is less well understood. Electrophysiological and tract tracing studies are revealing the functional connectivity of a more elaborate circuit through the avian cerebellum, which integrates optic flow with other sensory signals. Here we review the research supporting this framework and identify the cerebellar output centres, the lateral (CbL) and medial (CbM) cerebellar nuclei, as two key nodes with potentially distinct roles in flight control. The CbM receives bilateral optic flow information and projects to sites in the brainstem that suggest a primary role for flight control over time, such as during forward flight. The CbL receives monocular optic flow and other types of visual information. This site provides feedback to sensory areas throughout the brain and has a strong projection the nucleus ruber, which is known to have a dominant role in forelimb muscle control. This arrangement suggests primary roles for the CbL in the control of wing morphing and for rapid maneuvers.

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Adapted from Gutierrez-Ibanez et al. (Gutiérrez-Ibáñez et al. 2022). I Zonal organization of inputs from SpM and the pontine nuclei in the pigeon reconstructed from several injections of retrograde tracers in the OCb of pigeons. The lateral subdivision of SpM (SpMl) and PL project to zones A1 and E (yellow). The medial subdivision of SpM (SpMm) and PM project to zone A2 and C (green). J Circuit diagram showing direct and indirect sensory inputs to the OCb of birds. The lateral (green) and medial (yellow) subdivisions of SpM and the pontine nuclei form parallel pathways to the OCb—see text for details. Scale bars; A = 500 mm, B = 100 mm, D-H = 500 mm, I = 1 mm. GLv ventral geniculate nucleus, TeO Optic tectum, LPC nucleus laminaris precommissuralis

Fig. 5

Adapted from Arends and Zeigler (Arends and Zeigler 1991a) and Wylie et al. (2003a,b). VeS superior vestibular nucleus, PCV cerebellovestibular process, Ta tangential nucleus, VeM medial vestibular nucleus, VeD descending vestibular nucleus, pH prepositus hypoglossi, VDL dorsolateral vestibular nucleus, inf infracerebellar nucleus

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Acknowledgements

We thank Sylvia Heredia for illustrating Fig. 1. Our research on optic flow circuits and the cerebellum is funded by the Canadian Institutes of Health Research (FRN-159751 and PJT-169033).

Funding

This research was supported by funding to D.R.W. and D.L.A. from the Canadian Institutes of Health Research (CIHR).

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C.G.-I. and D.L.A. wrote the main manuscript text. D.R.W. prepared figures 2-3, and C.G.-I. prepared figures 4-6. All authors edited the manuscript.

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Correspondence to Douglas R. Wylie or Douglas L. Altshuler.

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Gutiérrez-Ibáñez, C., Wylie, D.R. & Altshuler, D.L. From the eye to the wing: neural circuits for transforming optic flow into motor output in avian flight. J Comp Physiol A 209, 839–854 (2023). https://doi.org/10.1007/s00359-023-01663-5

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  • DOI: https://doi.org/10.1007/s00359-023-01663-5

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