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

Gutiérrez-Ibáñez, Cristián; Wylie, Douglas R.; Altshuler, Douglas L.

doi:10.1007/s00359-023-01663-5

Cited by 5 publications

(4 citation statements)

References 120 publications

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“…The former pathway is hypothesized to process motion parallax while steering through complex environments; thus the oculomotor cerebellum likely integrates optic flow inputs with local motion signals and somatosensory information that are generated in multiple regions as the product of movement. Heightened activity within this region is best interpreted as a product of the spatial summation of these various inputs [5,24]. This hypothesis is congruent with the observation that avian species considered strong fliers tend to increase the size of folia VI-VII [48].…”

Section: (C) Cerebellum and Optic Flow Pathways: Significant Increase...supporting

confidence: 72%

“…An alternative prediction was proffered by Wylie et al [5] and Gutiérrez-Ibáñez [24] that the optic flow pathways-those pathways processing information of self-movement across the retina and motion parallax-will be the most active during flight. This hypothesis draws from previous behavioural studies showing that perturbations in visual flow patterns can affect the flightpath (see citations in [5]).…”

Section: Introductionmentioning

confidence: 99%

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Quantitative functional imaging of the pigeon brain: implications for the evolution of avian powered flight

Balanoff,

Ferrer,

Saleh

et al. 2024

Proc. R. Soc. B.

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The evolution of flight is a rare event in vertebrate history, and one that demands functional integration across multiple anatomical/physiological systems. The neuroanatomical basis for such integration and the role that brain evolution assumes in behavioural transformations remain poorly understood. We make progress by (i) generating a positron emission tomography (PET)-based map of brain activity for pigeons during rest and flight, (ii) using these maps in a functional analysis of the brain during flight, and (iii) interpreting these data within a macroevolutionary context shaped by non-avian dinosaurs. Although neural activity is generally conserved from rest to flight, we found significant increases in the cerebellum as a whole and optic flow pathways. Conserved activity suggests processing of self-movement and image stabilization are critical when a bird takes to the air, while increased visual and cerebellar activity reflects the importance of integrating multimodal sensory information for flight-related movements. A derived cerebellar capability likely arose at the base of maniraptoran dinosaurs, where volumetric expansion and possible folding directly preceded paravian flight. These data represent an important step toward establishing how the brain of modern birds supports their unique behavioural repertoire and provide novel insights into the neurobiology of the bird-like dinosaurs that first achieved powered flight.

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Section: (C) Cerebellum and Optic Flow Pathways: Significant Increase...supporting

confidence: 72%

Section: Introductionmentioning

confidence: 99%

Quantitative functional imaging of the pigeon brain: implications for the evolution of avian powered flight

Balanoff,

Ferrer,

Saleh

et al. 2024

Proc. R. Soc. B.

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“…LM and nBOR project to two regions of the cerebellum, the vestibulocerebellum and the oculomotor cerebellum [31][32][33][34][35][36][37]. Both regions are expected to have a role in flight control, but the projections to the oculomotor cerebellum suggest it may be especially well suited as the site of an internal forward model that requires a copy of the motor signal [38]. Specifically, optic flow signals from LM and nBOR in the oculomotor cerebellum can be integrated with descending projections related to motor planning and execution, originating in the nidopallium [39,40] and the anterior wulst [41] of the telencephalon.…”

Section: Discussionmentioning

confidence: 99%

Hummingbirds use distinct control strategies for forward and hovering flight

Baliga,

Dakin,

Wylie

et al. 2024

Proc. R. Soc. B.

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The detection of optic flow is important for generating optomotor responses to mediate retinal image stabilization, and it can also be used during ongoing locomotion for centring and velocity control. Previous work in hummingbirds has separately examined the roles of optic flow during hovering and when centring through a narrow passage during forward flight. To develop a hypothesis for the visual control of forward flight velocity, we examined the behaviour of hummingbirds in a flight tunnel where optic flow could be systematically manipulated. In all treatments, the animals exhibited periods of forward flight interspersed with bouts of spontaneous hovering. Hummingbirds flew fastest when they had a reliable signal of optic flow. All optic flow manipulations caused slower flight, suggesting that hummingbirds had an expected optic flow magnitude that was disrupted. In addition, upward and downward optic flow drove optomotor responses for maintaining altitude during forward flight. When hummingbirds made voluntary transitions to hovering, optomotor responses were observed to all directions. Collectively, these results are consistent with hummingbirds controlling flight speed via mechanisms that use an internal forward model to predict expected optic flow whereas flight altitude and hovering position are controlled more directly by sensory feedback from the environment.

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“…Alternatively, both tectal 58 and vestibulo-spinal neurons [59][60][61] receive sensory input from a wide variety of modalities 62 and may be involved in relevant computations. Lastly, the cerebellum integrates vestibular [63][64][65][66] , visual 67,68 , and lateral line inputs 69,70 , and controls posture in larval zebrafish 71 . Cerebellar input originates in part in the inferior olive, which has recently been shown to play a role in positional homeostasis in the yaw axis 72 .…”

Section: Multisensory Strategies To Regulate Elevationmentioning

confidence: 99%

Multisensory strategies for postural compensation after lateral line loss

Davis,

Zhu,

Schoppik

2024

Preprint

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To control elevation underwater, aquatic vertebrates integrate multisensory information (e.g., vestibular, visual, proprioceptive) to guide posture and swim kinematics. Here we characterized how larval zebrafish changed posture and locomotive strategies after imposed instability (decreased buoyancy) in the presence and absence of visual cues. We discovered that larvae sank more after acute loss of lateral line (flow-sensing) hair cells. In response, larvae engaged different compensatory strategies, depending on whether they were in the light or dark. In the dark, larvae swam more frequently, engaging their trunk to steer their nose up and climb more effectively. However, in the light, larvae climbed more often, engaging both pectoral fins and trunk to elevate. We conclude that larvae sense instability and use vestibular and visual information as available to control posture and trajectory. Our work is a step towards understanding the multisensory neural computations responsible for control strategies that allow orientation and navigation in depth.

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

Cited by 5 publications

References 120 publications

Quantitative functional imaging of the pigeon brain: implications for the evolution of avian powered flight

Quantitative functional imaging of the pigeon brain: implications for the evolution of avian powered flight

Hummingbirds use distinct control strategies for forward and hovering flight

Multisensory strategies for postural compensation after lateral line loss

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