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Molecular and cellular determinants of motor asymmetry in zebrafish.

ABSTRACT: Asymmetries in motor behavior, such as human hand preference, are observed throughout bilateria. However, neural substrates and developmental signaling pathways that impose underlying functional lateralization on a broadly symmetric nervous system are unknown. Here we report that in the absence of over-riding visual information, zebrafish larvae show intrinsic lateralized motor behavior that is mediated by a cluster of 60 posterior tuberculum (PT) neurons in the forebrain. PT neurons impose motor bias via a projection through the habenular commissure. Acquisition of left/right identity is disrupted by heterozygous mutations in mosaic eyes and mindbomb, genes that regulate Notch signaling. These results define the neuronal substrate for motor asymmetry in a vertebrate and support the idea that haploinsufficiency for genes in a core developmental pathway destabilizes left/right identity.

SUBMITTER: Horstick EJ

PROVIDER: S-EPMC7054361 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Molecular and cellular determinants of motor asymmetry in zebrafish.

Horstick Eric J EJ Bayleyen Yared Y Burgess Harold A HA

Nature communications 20200303 1

Asymmetries in motor behavior, such as human hand preference, are observed throughout bilateria. However, neural substrates and developmental signaling pathways that impose underlying functional lateralization on a broadly symmetric nervous system are unknown. Here we report that in the absence of over-riding visual information, zebrafish larvae show intrinsic lateralized motor behavior that is mediated by a cluster of 60 posterior tuberculum (PT) neurons in the forebrain. PT neurons impose moto ...[more]

PMID: 32127541

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Project description:Innate behavioral biases such as human handedness are a ubiquitous form of inter-individual variation that are not strictly hardwired into the genome and are influenced by diverse internal and external cues. Yet, genetic and environmental factors modulating behavioral variation remain poorly understood, especially in vertebrates. To identify genetic and environmental factors that influence behavioral variation, we take advantage of larval zebrafish light-search behavior. During light-search, individuals preferentially turn in leftward or rightward loops, in which directional bias is sustained and non-heritable. Our previous work has shown that bias is maintained by a habenula-rostral PT circuit and genes associated with Notch signaling. Here we use a medium-throughput recording strategy and unbiased analysis to show that significant individual to individual variation exists in wildtype larval zebrafish turning preference. We classify stable left, right, and unbiased turning types, with most individuals exhibiting a directional preference. We show unbiased behavior is not due to a loss of photo-responsiveness but reduced persistence in same-direction turning. Raising larvae at elevated temperature selectively reduces the leftward turning type and impacts rostral PT neurons, specifically. Exposure to conspecifics, variable salinity, environmental enrichment, and physical disturbance does not significantly impact inter-individual turning bias. Pharmacological manipulation of Notch signaling disrupts habenula development and turn bias individuality in a dose dependent manner, establishing a direct role of Notch signaling. Last, a mutant allele of a known Notch pathway affecter gene, gsx2, disrupts turn bias individuality, implicating that brain regions independent of the previously established habenula-rostral PT likely contribute to inter-individual variation. These results establish that larval zebrafish is a powerful vertebrate model for inter-individual variation with established neural targets showing sensitivity to specific environmental and gene signaling disruptions. Our results provide new insight into how variation is generated in the vertebrate nervous system.

Dataset Information

Molecular and cellular determinants of motor asymmetry in zebrafish.

Publications

Molecular and cellular determinants of motor asymmetry in zebrafish.

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