Freely-moving mice visually pursue prey using a retinal area with least optic flow

Holmgren, Carl; Stahr, Paul; Wallace, Damian J.; Voit, Kay-Michael; Matheson, Emily J; Sawiński, J; Bassetto, Giacomo; Kerr, Jason N. D.

doi:10.1101/2021.06.15.448520

Cited by 5 publications

(3 citation statements)

References 72 publications

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“…It will be interesting to determine whether jumping mice control their gaze to localize the platform on a specific subregion of the retina; i.e., whether there exists a retinal specialization for determining distance. In the case of prey capture, the image of the cricket is stabilized in the retinal region with the highest concentration of alpha-ganglion cells (Holmgren et al, 2021).…”

Section: Eye Movements During Distance Estimationmentioning

confidence: 99%

Distance estimation from monocular cues in an ethological visuomotor task

Parker

Abe

Beatie

et al. 2022

eLife

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In natural contexts, sensory processing and motor output are closely coupled, which is reflected in the fact that many brain areas contain both sensory and movement signals. However, standard reductionist paradigms decouple sensory decisions from their natural motor consequences, and head-fixation prevents the natural sensory consequences of self-motion. In particular, movement through the environment provides a number of depth cues beyond stereo vision that are poorly understood. To study the integration of visual processing and motor output in a naturalistic task, we investigated distance estimation in freely moving mice. We found that mice use vision to accurately jump across a variable gap, thus directly coupling a visual computation to its corresponding ethological motor output. Monocular eyelid suture did not affect gap jumping success, thus mice can use cues that do not depend on binocular disparity and stereo vision. Under monocular conditions, mice altered their head positioning and performed more vertical head movements, consistent with a shift from using stereopsis to other monocular cues, such as motion or position parallax. Finally, optogenetic suppression of primary visual cortex impaired task performance under both binocular and monocular conditions when optical fiber placement was localized to binocular or monocular zone V1, respectively. Together, these results show that mice can use monocular cues, relying on visual cortex, to accurately judge distance. Furthermore, this behavioral paradigm provides a foundation for studying how neural circuits convert sensory information into ethological motor output.

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Section: Eye Movements During Distance Estimationmentioning

confidence: 99%

Distance estimation from monocular cues in an ethological visuomotor task

Parker

Abe

Beatie

et al. 2022

eLife

View full text Add to dashboard Cite

show abstract

“…The copyright holder for this preprint this version posted October 1, 2021. ; https://doi.org/10.1101/2021.09.29.462468 doi: bioRxiv preprint exists a retinal specialization for determining distance. In the case of prey capture, the image of the cricket is stabilized in the retinal region with the highest concentration of alpha-ganglion cells (Holmgren et al, 2021).…”

Section: Eye Movements During Distance Estimationmentioning

confidence: 99%

Distance estimation from monocular cues in an ethological visuomotor task

Parker

Abe

et al. 2021

Preprint

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In natural contexts, sensory processing and motor output are closely coupled, which is reflected in the fact that many brain areas contain both sensory and movement signals. However, standard reductionist paradigms decouple sensory decisions from their natural motor consequences, and head-fixation prevents the natural sensory consequences of self-motion. In particular, movement through the environment provides a number of depth cues beyond stereo vision that are poorly understood. To study the integration of visual processing and motor output in a naturalistic task, we investigated distance estimation in freely moving mice. We found that mice use vision to accurately jump across a variable gap, thus directly coupling a visual computation to its corresponding ethological motor output. Monocular eyelid suture did not affect performance, thus mice can use cues that do not depend on binocular disparity and stereo vision. Under monocular conditions, mice performed more vertical head movements, consistent with the use of motion parallax cues, and optogenetic suppression of primary visual cortex impaired task performance. Together, these results show that mice can use monocular cues, relying on visual cortex, to accurately judge distance. Furthermore, this behavioral paradigm provides a foundation for studying how neural circuits convert sensory information into ethological motor output.

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“…This may be the reason that nearly all vertebrates utilize a "saccade and fixate" strategy whereby gaze is rapidly moved to a new location and then kept stable by way of a gaze stabilization reflexes such as the vestibular ocular reflex (VOR) e.g. [3]. These gaze stabilization mechanisms are phylogenically ancient, with evidence for compensatory eye movements stretching back to the origin of bony fish approximately 450 million years ago [1,4].…”

Section: Introductionmentioning

confidence: 99%

Retinal optic flow during natural locomotion

et al. 2022

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We examine the structure of the visual motion projected on the retina during natural locomotion in real world environments. Bipedal gait generates a complex, rhythmic pattern of head translation and rotation in space, so without gaze stabilization mechanisms such as the vestibular-ocular-reflex (VOR) a walker’s visually specified heading would vary dramatically throughout the gait cycle. The act of fixation on stable points in the environment nulls image motion at the fovea, resulting in stable patterns of outflow on the retinae centered on the point of fixation. These outflowing patterns retain a higher order structure that is informative about the stabilized trajectory of the eye through space. We measure this structure by applying the curl and divergence operations on the retinal flow velocity vector fields and found features that may be valuable for the control of locomotion. In particular, the sign and magnitude of foveal curl in retinal flow specifies the body’s trajectory relative to the gaze point, while the point of maximum divergence in the retinal flow field specifies the walker’s instantaneous overground velocity/momentum vector in retinotopic coordinates. Assuming that walkers can determine the body position relative to gaze direction, these time-varying retinotopic cues for the body’s momentum could provide a visual control signal for locomotion over complex terrain. In contrast, the temporal variation of the eye-movement-free, head-centered flow fields is large enough to be problematic for use in steering towards a goal. Consideration of optic flow in the context of real-world locomotion therefore suggests a re-evaluation of the role of optic flow in the control of action during natural behavior.

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Freely-moving mice visually pursue prey using a retinal area with least optic flow

Cited by 5 publications

References 72 publications

Distance estimation from monocular cues in an ethological visuomotor task

Distance estimation from monocular cues in an ethological visuomotor task

Distance estimation from monocular cues in an ethological visuomotor task

Retinal optic flow during natural locomotion

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