Brain and Behavioral Asymmetry: A Lesson From Fish

Petrazzini, Maria Elena Miletto; Sovrano, Valeria Anna; Vallortígara, Giorgio; Messina, Andrea

doi:10.3389/fnana.2020.00011

Cited by 53 publications

(43 citation statements)

References 254 publications

(338 reference statements)

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“…In the last twenty years, zebrafish ( Danio rerio ) has become a prominent model to study the molecular mechanisms of brain lateralization (Carl et al., 2007; Concha, Burdine, Russell, Schier, & Wilson, 2000; Duboc, Dufourcq, Blader, & Roussigné, 2015; Liang et al., 2000; Miletto Petrazzini, Sovrano, Vallortigara, & Messina, 2020). Research with zebrafish established that vertebrates laterality seems to be guided by four major pathways (nodal, fibroblast growth factors, notch and Wnt/beta catenin), which are involved in the positioning of some genes ( ndr2 , lefty 1 and pitx2 ) on the left side of the forming neural tube (Carl et al., 2007; Concha et al., 2000; Essner, Amack, Nyholm, Harris, & Yost, 2005; Hüsken & Carl, 2013; Liang et al., 2000; Raya et al., 2003; Regan, Concha, Roussigne, Russell, & Wilson, 2009) and contributing to the generation of zebrafish thalamus asymmetries with the positioning of kctd12.1/leftover in the left and of ktcd8/dexter and ktcd12.2/right‐on in the right primordium of habenular nuclei (Gamse et al., 2005; Gamse, Thisse, Thisse, & Halpern, 2003).…”

Section: Introductionmentioning

confidence: 99%

Asymmetric distribution of pallial‐expressed genes in zebrafish (Danio rerio)

Messina

Boiti

Vallortígara

2020

Eur J of Neuroscience

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The left and right distribution of a set of twenty‐six genes in the zebrafish pallium was examined by RT‐qPCR experiments. The analysis comprised four general pallial markers (eomesa, emx2, emx3 and prox1); eight genes, dapper1, htr3a, htr3b, htr4, id2, ndr2, pkcβ and lmo4, that have been described as asymmetric distributed in the brain of mammals (human and mouse); six genes, arrb2, auts2, baiap2, fez1, gap43 and robo1, asymmetrically distributed in the mammalian cortex, that have been associated with autism in humans; and, eight genes, baz1b, fzd9, limk1, tubgcp5, cyfip1, grik1a, nipa1 and nipa2, which have been associated with developmental dyscalculia, a brain disability linked to brain laterality in humans. We found a leftward bias in the expression of 10 genes (dapper1, htr3a, htr3b, htr4, id2, ndr2, pkcß, auts2, baiap2 and grik1a) and a rightward bias for 5 genes (lmo4, arrb2, fez1, gap43, robo1) in agreement with the data reported in mammals. We also found a rightward lateralization for nipa1 and nipa2, whereas the remaining genes (eomesa, emx2, emx3, prox1, baz1b, cyfip1, fzd9, limk1 and tubgpc5) were bilaterally distributed. These findings suggest a basic homology in the asymmetric expression of several pallial vertebrate genes.

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Section: Introductionmentioning

confidence: 99%

Asymmetric distribution of pallial‐expressed genes in zebrafish (Danio rerio)

Messina

Boiti

Vallortígara

2020

Eur J of Neuroscience

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“…Asymmetric behaviors have been described in a range of metazoans (Güntürkün et al, 2020) . Among the chordates, the consequences of disruptions to CNS left-right asymmetry on behavior has been detailed most extensively in zebrafish (Miletto Petrazzini et al, 2020). Notably, zebrafish larvae show a similar response to Cion a larvae in response to dimming light --circular swimming.…”

Section: Discussionmentioning

confidence: 99%

Left/right asymmetry disruptions and mirror-image reversals to behavior and brain anatomy inCiona

Mj¹,

Bostwick

A³

et al. 2021

Preprint

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Left-right asymmetries are a common feature of metazoan nervous systems. This is particularly pronounced in the comparatively simple larval central nervous system (CNS) of the tunicate Ciona , whose swimming tadpole larva shows a clear chordate ground plan. While common pathway elements for specifying the left-right axis are found in the chordates, particularly a requirement for Nodal signaling, Ciona differs from its vertebrate cousins by specifying its axis at the neurula stage, rather than at gastrula. Additionally, Ciona , and other ascidians, have a requirement for an intact chorionic membrane for proper left/right specification. We present here results showing that left-right asymmetry disruptions caused by removal of the chorion (dechorionation) are highly variable and present throughout the Ciona larval nervous system. While previous studies have documented disruptions to the conspicuously asymmetric sensory systems in the anterior brain vesicle, we document asymmetries in seemingly symmetric structures such as the posterior brain vesicle and motor ganglion. Moreover, defects caused by dechorionation include misplaced or absent neuron classes, loss of asymmetric gene expression, aberrant synaptic connectivity, and abnormal behaviors. In the motor ganglion, a brain structure that has been equated with the vertebrate hindbrain, we find that despite the apparent left/right symmetric distribution of interneurons and motor neurons, AMPA receptors are expressed exclusively on the left side, which equates with asymmetric swimming behaviors. We also find that within a population of dechorionated larvae, there is a small percentage with apparently normal left-right specification, and approximately equal population with inverted (mirror-image) asymmetry. We present a method based on a behavioral assay for isolating these larvae. When these two classes of larvae (normal and inverted) are assessed in a light dimming assay they display mirror-image behaviors, with normal larvae responding with counterclockwise swims, while inverted larvae respond with clockwise swims.Our findings highlight the importance of left-right specification pathways not only for proper CNS anatomy, but also for correct synaptic connectivity and behavior.

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“…It is possible, as Chiandetti and Vallortigara [81] have suggested, that the early effect of light influences the development of visual lateralization by modulating the activity of genes expressed in the development of lateralization. This could involve aspects of the Nodal cascade or be associated with nerve growth factor, which has a role in left-right patterning and a vital role in axial rotation of the early embryo [83]; also see [84] for genes involved in the expression of lateralization in fish.…”

Section: Asymmetry Of Development Of the Chick Embryomentioning

confidence: 99%

Asymmetry of Motor Behavior and Sensory Perception: Which Comes First?

Rogers

2020

Symmetry

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By examining the development of lateralization in the sensory and motor systems of the human fetus and chick embryo, this paper debates which lateralized functions develop first and what interactions may occur between the different sensory and motor systems during development. It also discusses some known influences of inputs from the environment on the development of lateralization, particularly the effects of light exposure on the development of visual and motor lateralization in chicks. The effects of light on the human fetus are related in this context. Using the chick embryo as a model to elucidate the genetic and environmental factors involved in development of lateralization, some understanding has been gained about how these lateralized functions emerge. At the same time, the value of carrying out much more research on the development of the various types of lateralization has become apparent.

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Brain and Behavioral Asymmetry: A Lesson From Fish

Cited by 53 publications

References 254 publications

Asymmetric distribution of pallial‐expressed genes in zebrafish (Danio rerio)

Asymmetric distribution of pallial‐expressed genes in zebrafish (Danio rerio)

Left/right asymmetry disruptions and mirror-image reversals to behavior and brain anatomy inCiona

Asymmetry of Motor Behavior and Sensory Perception: Which Comes First?

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