Pablo Oteíza

Max Planck Institute for Ornithology

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Florian Engert

Harvard University

Iris Odstrcil

Harvard University

Rubén Portugués

Technical University of Munich

Carl‐Philipp Heisenberg

Institute of Science and Technology Austria

Miguel L. Concha

University of Chile

Mathias Köppen

Instituto Gulbenkian de Ciência

Maxim Nikitchenko

Harvard University

Richard Schalek

Harvard University

Martin Haesemeyer

The Ohio State University

Mariela D. Petkova

Harvard University

Cooperative Institutions

Harvard University

Harvard University Press

University of Chile

Instituto de Neurociencia Biomédica

Max Planck Institute of Molecular Cell Biology and Genetics

The University of Tokyo

Center for Pain and the Brain

Consejo Superior de Investigaciones Científicas

Max Planck Society

Meiji University

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Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Iris Odstrcil Mariela D. Petkova Martin Haesemeyer Jonathan Boulanger-Weill Maxim Nikitchenko

Abstract All animals need to differentiate between exafferent stimuli, which are caused by the environment, and reafferent stimuli, which are caused by their own movement. In the case of mechanosensation in aquatic animals, the exafferent inputs are water vibrations in the animal’s proximity, which need to be distinguished from the reafferent inputs arising from fluid drag due to locomotion. Both of these inputs are detected by the lateral line, a collection of mechanosensory organs distributed along the surface of the body. In this study, we characterize in detail how the hair cells, which are the receptor cells of the lateral line, discriminate between such reafferent and exafferent signals in zebrafish larvae. Using dye labeling of the lateral line nerve, we visualize two parallel descending inputs that can influence lateral line sensitivity. We combine functional imaging with ultra-structural EM circuit reconstruction to show that cholinergic signals originating from the hindbrain transmit efference copies that cancel out self-generated reafferent stimulation during locomotion, and that dopaminergic signals from the hypothalamus may have a role in threshold modulation both in response to locomotion and salient stimuli. We further gain direct mechanistic insight into the core components of this circuit by loss-of-function perturbations using targeted ablations and gene knockouts. We propose that this simple circuit is the core implementation of mechanosensory reafferent suppression in these young animals and that it might form the first instantiation of state-dependent modulation found at later stages in development.

mechanosensation

Hindbrain

Lateral line

10.1101/2021.05.04.442674

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Citations (2)

Evolution of sensory systems

Current Opinion in Neurobiology (2021)

Pablo Oteíza Maude W. Baldwin

10.1016/j.conb.2021.08.005

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Citations (32)

Functional and Ultrastructural Analysis of Reafferent Mechanosensation in Larval Zebrafish

SSRN Electronic Journal (2021)

Iris Odstrcil Mariela D. Petkova Martin Haesemeyer Jonathan Boulanger Maxim Nikitchenko

All animals need to differentiate between exafferent stimuli, which are caused by the environment, and reafferent stimuli, which are caused by their own movement. In the case of mechanosensation in aquatic animals, the exafferent inputs are water vibrations in the animalâ€™s proximity, which need to be distinguished from the reafferent inputs arising from fluid drag due to locomotion. Both of these inputs are detected by the lateral line, a collection of mechanosensory organs distributed along the surface of the body.In this study, we characterize in detail how the hair cells, which are the receptor cells of the lateral line, discriminate between such reafferent and exafferent signals in zebrafish larvae. Using dye labeling of the lateral line nerve, we visualize two parallel descending inputs that can influence lateral line sensitivity. We combine functional imaging with ultra-structural EM circuit reconstruction to show that cholinergic signals originating from the hindbrain transmit efference copies that cancel out self-generated reafferent stimulation during locomotion, and that dopaminergic signals from the hypothalamus may have a role in threshold modulation both in response to locomotion and salient stimuli. We further gain direct mechanistic insight into the core components of this circuit by loss-of-function perturbations using targeted ablations and gene knockouts.We propose that this simple circuit is the core implementation of mechanosensory reafferent suppression in these young animals and that it might form the first instantiation of state-dependent modulation found at later stages in development.

mechanosensation

10.2139/ssrn.3845002

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Citations (0)

Early origin of sweet perception in the songbird radiation

Science (2021)

Yasuka Toda Meng‐Ching Ko Qiaoyi Liang Eliot T. Miller Alejandro Rico‐Guevara

From savory to sweet Seeing a bird eat nectar from a flower is a common sight in our world. The ability to detect sugars, however, is not ancestral in the bird lineage, where most species were carnivorous. Toda et al. looked at receptors within the largest group of birds, the passerines or songbirds, and found that the emergence of sweet detection involved a single shift in a receptor for umami (see the Perspective by Barker). This ancient change facilitated sugar detection not just in nectar feeding birds, but also across the songbird group, and in a way that was different from, though convergent with, that in hummingbirds. Science , abf6505, this issue p. 226 ; see also abj6746, p. 154

Songbird

10.1126/science.abf6505

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Citations (46)

S10-05 Linking organ formation to left–right patterning in the embryonic zebrafish

Mechanisms of Development (2009)

Pablo Oteíza Carmen G. Lemus Mathias Köppen Karina Palma Michael Krieg

10.1016/j.mod.2009.06.970

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Citations (1)

A novel mechanism for mechanosensory-based rheotaxis in larval zebrafish

Nature (2017)

Pablo Oteíza Iris Odstrcil George Lauder Rubén Portugués Florian Engert

Danio

Lateral line

10.1038/nature23014

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Citations (170)

Swimming Against the Flow

TheScienceBreaker (2018)

Pablo Oteíza

10.25250/thescbr.brk088

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Citations (0)

Erratum: A novel mechanism for mechanosensory-based rheotaxis in larval zebrafish

Nature (2017)

Pablo Oteíza Iris Odstrcil George Lauder Rubén Portugués Florian Engert

10.1038/nature23895

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Citations (1)

RE-1 Silencer of Transcription/Neural Restrictive Silencer Factor Modulates Ectodermal Patterning duringXenopusDevelopment

Journal of Neuroscience (2006)

Patricio Olguı́n Pablo Oteíza Eduardo Andión Gamboa José Luis Gómez-Skármeta Manuel Kukuljan

RE-1 silencer of transcription/neural restrictive silencer factor (REST/NRSF), a transcriptional repressor, binds to the RE-1 element present in many vertebrate genes. In vitro studies indicate that REST/NRSF plays important roles in several stages of neural development. However, a full understanding of its physiological function requires in vivo approaches. We find that impairment of REST/NRSF function in Xenopus embryos leads to the perturbation of neural tube, cranial ganglia, and eye development. The origin of these defects is the abnormal patterning of the ectoderm during gastrulation. Interference of REST/NRSF function during the late blastula stage leads to an expansion of the neural plate, concomitant with a decrease of the expression of epidermal keratin and neural crest markers. Furthermore, neurogenesis proceeds abnormally, with loss of the expression of proneural, neurogenic, and neuronal genes. The interference of REST/NRSF mimics several features associated with a decreased bone morphogenetic protein (BMP) function and counteracts some effects of BMP4 misexpression. Our results indicate that REST/NRSF function is required in vivo for the acquisition of specific ectodermal cell fates.

Silencer

Neural Development

Blastula

10.1523/jneurosci.5037-05.2006

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Citations (27)

Planar cell polarity signalling regulates cell adhesion properties in progenitors of the zebrafish laterality organ

Development (2010)

Pablo Oteíza Mathias Köppen Michael Krieg Eduardo Pulgar Cecilia Farias

Organ formation requires the precise assembly of progenitor cells into a functional multicellular structure. Mechanical forces probably participate in this process but how they influence organ morphogenesis is still unclear. Here, we show that Wnt11- and Prickle1a-mediated planar cell polarity (PCP) signalling coordinates the formation of the zebrafish ciliated laterality organ (Kupffer's vesicle) by regulating adhesion properties between organ progenitor cells (the dorsal forerunner cells, DFCs). Combined inhibition of Wnt11 and Prickle1a reduces DFC cell-cell adhesion and impairs their compaction and arrangement during vesicle lumen formation. This leads to the formation of a mis-shapen vesicle with small fragmented lumina and shortened cilia, resulting in severely impaired organ function and, as a consequence, randomised laterality of both molecular and visceral asymmetries. Our results reveal a novel role for PCP-dependent cell adhesion in coordinating the supracellular organisation of progenitor cells during vertebrate laterality organ formation.

Progenitor

10.1242/dev.049981

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Citations (67)