Low Gain Values of the Vestibulo-Ocular Reflex Can Optimize Retinal Image Slip

Glasauer, Stefan

doi:10.3389/fneur.2022.897293

“…Prerequisite to this homeostatic plasticity is the variability of the naïve OKR before training. A comparably variable inter-individual performance has been observed for the goldfish [ 58 ] and Xenopus tadpole OKR [ 55 ], as well as for the Xenopus VOR [ 59 ], and is likely related to intrinsic sensory–motor noise levels in the system as indicated in the latter study. This also includes variations in retinal sensitivity to the stimulus, as well as different muscle strengths and differences in the activity levels in the underlying neuronal circuits.…”

Section: Discussionmentioning

confidence: 83%

Homeostatic plasticity of eye movement performance in Xenopus tadpoles following prolonged visual image motion stimulation

Forsthofer

¹

2022

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Visual image motion-driven ocular motor behaviors such as the optokinetic reflex (OKR) provide sensory feedback for optimizing gaze stability during head/body motion. The performance of this visuo-motor reflex is subject to plastic alterations depending on requirements imposed by specific eco-physiological or developmental circumstances. While visuo-motor plasticity can be experimentally induced by various combinations of motion-related stimuli, the extent to which such evoked behavioral alterations contribute to the behavioral demands of an environment remains often obscure. Here, we used isolated preparations of Xenopus laevis tadpoles to assess the extent and ontogenetic dependency of visuo-motor plasticity during prolonged visual image motion. While a reliable attenuation of large OKR amplitudes can be induced already in young larvae, a robust response magnitude-dependent bidirectional plasticity is present only at older developmental stages. The possibility of older larvae to faithfully enhance small OKR amplitudes coincides with the developmental maturation of inferior olivary–Purkinje cell signal integration. This conclusion was supported by the loss of behavioral plasticity following transection of the climbing fiber pathway and by the immunohistochemical demonstration of a considerable volumetric extension of the Purkinje cell dendritic area between the two tested stages. The bidirectional behavioral alterations with different developmental onsets might functionally serve to standardize the motor output, comparable to the known differential adaptability of vestibulo-ocular reflexes in these animals. This homeostatic plasticity potentially equilibrates the working range of ocular motor behaviors during altered visuo-vestibular conditions or prolonged head/body motion to fine-tune resultant eye movements.

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“…In both VOR and OKR, training stimuli induce motor output homeostasis rather than stronger compensation 56,57 . Theoretical studies corroborate this finding, and suggest that consistency may be preferred, and full compensation may not be necessary to minimize retinal image slip under naturalistic conditions 58 .…”

Section: Directionality In Xenopus Okrmentioning

confidence: 56%

Bilateral retinofugal pathfinding impairments limit behavioral compensation in near-congenital one-eyedXenopus laevis

Forsthofer,

Gordy,

Kolluri

et al. 2023

Preprint

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To generate a coherent visual percept, information from both eyes must be appropriately transmitted into the brain, where binocular integration forms the substrate for visuomotor behaviors. To establish the anatomical substrate for binocular integration, the presence of bilateral eyes and interaction of both optic nerves during retinotectal development play a key role. However, the extent to which embryonic monocularly derived visual circuits can convey visuomotor behaviors is unknown. In this study, we assessed the retinotectal anatomy and visuomotor performance of embryonically generated one-eyed tadpoles. In one-eyed animals, the axons of retinal ganglion cells from the singular remaining eye exhibited striking irregularities in their central projections in the brain, generating a non-canonical ipsilateral retinotectal projection. This data is indicative of impaired pathfinding abilities. We further show that these novel projections are correlated with an impairment of behavioral compensation for the loss of one eye.

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“…In both VOR and OKR, training stimuli induce motor output homeostasis rather than stronger compensation (Dietrich and Straka 2016;Forsthofer and Straka 2022). Theoretical studies corroborate this finding, and suggest that consistency may be preferred, and full compensation may not be necessary to minimize retinal image slip under naturalistic conditions (Glasauer and Straka 2022).…”

Section: Directionality In Xenopus Okrmentioning

confidence: 72%

Bilateral Retinofugal Pathfinding Impairments Limit Behavioral Compensation in Near-Congenital One-EyedXenopus laevis

Forsthofer,

Gordy,

Kolluri

et al. 2023

eNeuro

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To generate a coherent visual percept, information from both eyes must be appropriately transmitted into the brain, where binocular integration forms the substrate for visuomotor behaviors. To establish the anatomical substrate for binocular integration, the presence of bilateral eyes and interaction of both optic nerves during retinotectal development play a key role. However, the extent to which embryonic monocularly derived visual circuits can convey visuomotor behaviors is unknown. In this study, we assessed the retinotectal anatomy and visuomotor performance of embryonically generated one-eyed tadpoles. In one-eyed animals, the axons of retinal ganglion cells from the singular remaining eye exhibited striking irregularities in their central projections in the brain, generating a non-canonical ipsilateral retinotectal projection. This data is indicative of impaired pathfinding abilities. We further show that these novel projections are correlated with an impairment of behavioral compensation for the loss of one eye.Significance StatementThis study suggests that embryonic sensory imbalance has more far-reaching effects on function compared to acute loss in already established circuits. More generally, bilaterality of sensory organs is the norm across all vertebrates as well as many invertebrates, and our results contribute to a general understanding of how developmental programs, as well as behaviours reliant on them, pivotally depend on the presence of sensory inputs from both body sides.

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Low Gain Values of the Vestibulo-Ocular Reflex Can Optimize Retinal Image Slip

Cited by 3 publications

References 30 publications

Homeostatic plasticity of eye movement performance in Xenopus tadpoles following prolonged visual image motion stimulation

Homeostatic plasticity of eye movement performance in Xenopus tadpoles following prolonged visual image motion stimulation

Bilateral retinofugal pathfinding impairments limit behavioral compensation in near-congenital one-eyedXenopus laevis

Bilateral Retinofugal Pathfinding Impairments Limit Behavioral Compensation in Near-Congenital One-EyedXenopus laevis

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