Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish

Odstrcil, Iris; Petkova, Mariela D.; Haesemeyer, Martin; Boulanger-Weill, Jonathan; Nikitchenko, Maxim; Gagnon, James A.; Oteíza, Pablo; Schalek, Richard; Peleg, Adi; Portugues, Rubén; Lichtman, Jeff W.; Engert, Florian

doi:10.1016/j.cub.2021.11.007

Cited by 14 publications

(14 citation statements)

References 92 publications

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“…For example, active-flow sensing by cavefish depends on detecting reafferent signals while swimming ( Tan et al, 2011 ). Increased reliance on self-generated fluid motion ( Odstrcil et al, 2022 ; Patton et al, 2010 ; Teyke, 1985 ) is divergent from our current understanding of the CD’s role in predictive motor signaling in the lateral line ( Lunsford et al, 2019 ; Pichler and Lagnado, 2020 ).…”

Section: Introductionmentioning

confidence: 85%

Evolutionary convergence of a neural mechanism in the cavefish lateral line system

Lunsford

Paz

Keene

et al. 2022

eLife

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Animals can evolve dramatic sensory functions in response to environmental constraints, but little is known about the neural mechanisms underlying these changes. The Mexican tetra, Astyanax mexicanus, is a leading model to study genetic, behavioral, and physiological evolution by comparing eyed surface populations and blind cave populations. We compared neurophysiological responses of posterior lateral line afferent neurons and motor neurons across A. mexicanus populations to reveal how shifts in sensory function may shape behavioral diversity. These studies indicate differences in intrinsic afferent signaling and gain control across populations. Elevated endogenous afferent activity identified a lower response threshold in the lateral line of blind cavefish relative to surface fish leading to increased evoked potentials during hair cell deflection in cavefish.. We next measured the effect of inhibitory corollary discharges from hindbrain efferent neurons onto afferents during locomotion. We discovered that three independently-derived cavefish populations have evolved persistent afferent activity during locomotion, suggesting for the first time that partial loss of function in the efferent system can be an evolutionary mechanism for neural adaptation of a vertebrate sensory system.

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Section: Introductionmentioning

confidence: 85%

Evolutionary convergence of a neural mechanism in the cavefish lateral line system

Lunsford

Paz

Keene

et al. 2022

eLife

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“…Also, manual reconstructions of connectivity are labor-intensive and costly. Thus, with the exception of the olfactory bulb work mentioned above 11 , 13 , EM-based circuit analysis in zebrafish has been limited to few cells in specific areas of the nervous system 10 , 17 – 21 . One of our aims is to make connectomic data and computational tools available to the entire zebrafish community.…”

Section: Mainmentioning

confidence: 99%

Automated synapse-level reconstruction of neural circuits in the larval zebrafish brain

Svara¹,

Förster

Kubo

et al. 2022

Nat Methods

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Dense reconstruction of synaptic connectivity requires high-resolution electron microscopy images of entire brains and tools to efficiently trace neuronal wires across the volume. To generate such a resource, we sectioned and imaged a larval zebrafish brain by serial block-face electron microscopy at a voxel size of 14 × 14 × 25 nm3. We segmented the resulting dataset with the flood-filling network algorithm, automated the detection of chemical synapses and validated the results by comparisons to transmission electron microscopic images and light-microscopic reconstructions. Neurons and their connections are stored in the form of a queryable and expandable digital address book. We reconstructed a network of 208 neurons involved in visual motion processing, most of them located in the pretectum, which had been functionally characterized in the same specimen by two-photon calcium imaging. Moreover, we mapped all 407 presynaptic and postsynaptic partners of two superficial interneurons in the tectum. The resource developed here serves as a foundation for synaptic-resolution circuit analyses in the zebrafish nervous system.

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“…For example, active-flow sensing by cavefish depends on detecting reafferent signals while swimming (Tan et al, 2011). Increased reliance on self-generated fluid motion (Odstrcil et al, 2021;Patton et al, 2010;Teyke, 1985) is divergent from our current understanding of the CD's role in predictive motor signaling in the lateral line (Lunsford et al, 2019;Pichler & Lagnado, 2020).…”

Section: Introductionmentioning

confidence: 98%

Evolutionary convergence of a neural mechanism in the cavefish lateral line system

Lunsford

Paz

Keene

et al. 2022

Preprint

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Animals can evolve dramatic sensory functions in response to environmental constraints, but little is known about the neural mechanisms underlying these changes. The Mexican tetra, Astyanax mexicanus, is a leading model to study genetic, behavioral, and physiological evolution by comparing eyed surface populations and blind cave populations. We compared neurophysiological responses of posterior lateral line afferent neurons and motor neurons across A. mexicanus populations to reveal how shifts in sensory function may shape behavioral diversity. These studies indicate differences in intrinsic afferent signaling and gain control across populations. Elevated endogenous afferent activity identified a lower response threshold in the lateral line of blind cavefish relative to surface fish. We next measured the effect of inhibitory corollary discharges from hindbrain efferent neurons onto afferents during locomotion. We discovered that three independently-derived cavefish populations have evolved persistent afferent activity during locomotion, suggesting for the first time that regression of the efferent system can be an evolutionary mechanism for neural adaptation of a vertebrate sensory system.

show abstract

Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish

Cited by 14 publications

References 92 publications

Evolutionary convergence of a neural mechanism in the cavefish lateral line system

Evolutionary convergence of a neural mechanism in the cavefish lateral line system

Automated synapse-level reconstruction of neural circuits in the larval zebrafish brain

Evolutionary convergence of a neural mechanism in the cavefish lateral line system

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