Patterning of brain precursors in ascidian embryos

Esposito, Roberto; Yasuo, Hitoyoshi; Sirour, Cathy; Palladino, Antonio; Hudson, C. S.

doi:10.1242/dev.142307

Cited by 12 publications

(8 citation statements)

References 49 publications

(59 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The gene Otx , which is expressed in the forebrain and midbrain of vertebrates ( Boyl et al, 2001 ), is expressed in Ciona in both the aBV and pBV ( Imai et al, 2002 ; Hudson et al, 2003 ; Ikuta and Saiga, 2007 ), while a number of the vertebrate forebrain markers are expressed only in the aBV lineage. This includes the genes Dmrt1 ( Tresser et al, 2010 ; Wagner and Levine, 2012 ; Kikkawa et al, 2013 ), as well as Lhx5 , Six3 , and Gsx2 ( Mazet et al, 2005 ; Moret et al, 2005 ; Esposito et al, 2017 ; Reeves et al, 2017 ), all of which play essential roles in vertebrate forebrain development ( Toresson et al, 2000 ; Lagutin, 2003 ; Peng, 2006 ; Kirkeby et al, 2012 ). While Gsx2 is also expressed in the pBV, this is only in later stages of development (tailbud stages).…”

Section: Resultsmentioning

confidence: 99%

Fold Change Detection in Visual Processing

Borba

Kourakis

Schwennicke

et al. 2021

Front. Neural Circuits

View full text Add to dashboard Cite

Visual processing transforms the complexities of the visual world into useful information. Ciona, an invertebrate chordate and close relative of the vertebrates, has one of the simplest nervous systems known, yet has a range of visuomotor behaviors. This simplicity has facilitated studies linking behavior and neural circuitry. Ciona larvae have two distinct visuomotor behaviors – a looming shadow response and negative phototaxis. These are mediated by separate neural circuits that initiate from different clusters of photoreceptors, with both projecting to a CNS structure called the posterior brain vesicle (pBV). We report here that inputs from both circuits are processed to generate fold change detection (FCD) outputs. In FCD, the behavioral response scales with the relative fold change in input, but is invariant to the overall magnitude of the stimulus. Moreover, the two visuomotor behaviors have fundamentally different stimulus/response relationships – indicative of differing circuit strategies, with the looming shadow response showing a power relationship to fold change, while the navigation behavior responds linearly. Pharmacological modulation of the FCD response points to the FCD circuits lying outside of the visual organ (the ocellus), with the pBV being the most likely location. Consistent with these observations, the connectivity and properties of pBV interneurons conform to known FCD circuit motifs, but with different circuit architectures for the two circuits. The negative phototaxis circuit forms a putative incoherent feedforward loop that involves interconnecting cholinergic and GABAergic interneurons. The looming shadow circuit uses the same cholinergic and GABAergic interneurons, but with different synaptic inputs to create a putative non-linear integral feedback loop. These differing circuit architectures are consistent with the behavioral outputs of the two circuits. Finally, while some reports have highlighted parallels between the pBV and the vertebrate midbrain, suggesting a common origin for the two, others reports have disputed this, suggesting that invertebrate chordates lack a midbrain homolog. The convergence of visual inputs at the pBV, and its putative role in visual processing reported here and in previous publications, lends further support to the proposed common origin of the pBV and the vertebrate midbrain.

show abstract

Section: Resultsmentioning

confidence: 99%

Fold Change Detection in Visual Processing

Borba

Kourakis

Schwennicke

et al. 2021

Front. Neural Circuits

View full text Add to dashboard Cite

show abstract

“…Their fine structure and the projection of the outer segments into the cup-shaped pigment cell have been analyzed by confocal and electron microscopy (Horie et al, 2008;Salas et al, 2018;Kourakis et al, 2019). The promoter of the ParaHox Gsx gene directs specifically the reporter expression in both the a9.33 and A9.14 cell lineages proposed as PRC precursors (Esposito, 2014;Oonuma et al, 2016;Esposito et al, 2017;Palladino, 2017). As described in Supplementary Figure 1, Gsx expression precedes that of Oc in these cells.…”

Section: Ascidian Onecut Functions In Ocellus Differentiationmentioning

confidence: 99%

Onecut Regulates Core Components of the Molecular Machinery for Neurotransmission in Photoreceptor Differentiation

Vassalli

Colantuono

Nittoli

et al. 2021

Front. Cell Dev. Biol.

View full text Add to dashboard Cite

Photoreceptor cells (PRC) are neurons highly specialized for sensing light stimuli and have considerably diversified during evolution. The genetic mechanisms that underlie photoreceptor differentiation and accompanied the progressive increase in complexity and diversification of this sensory cell type are a matter of great interest in the field. A role of the homeodomain transcription factor Onecut (Oc) in photoreceptor cell formation is proposed throughout multicellular organisms. However, knowledge of the identity of the Oc downstream-acting factors that mediate specific tasks in the differentiation of the PRC remains limited. Here, we used transgenic perturbation of the Ciona robusta Oc protein to show its requirement for ciliary PRC differentiation. Then, transcriptome profiling between the trans-activation and trans-repression Oc phenotypes identified differentially expressed genes that are enriched in exocytosis, calcium homeostasis, and neurotransmission. Finally, comparison of RNA-Seq datasets in Ciona and mouse identifies a set of Oc downstream genes conserved between tunicates and vertebrates. The transcription factor Oc emerges as a key regulator of neurotransmission in retinal cell types.

show abstract

“…Most significantly, Otx , which is expressed in the forebrain and midbrain of vertebrates (Boyl et al, 2001), is expressed in Ciona in both the aBV and pBV (Hudson et al, 2003;Ikuta and Saiga, 2007;Imai et al, 2002), while a number of the vertebrate forebrain makers are expressed only in the aBV lineage. This includes the genes Dmrt1 (Kikkawa et al, 2013;Tresser et al, 2010;Wagner and Levine, 2012), as well as the genes Lhx5 , Six3 , and Gsx2 (Reeves et al, 2017;Mazet et al, 2005;Moret et al, 2005b;Esposito et al, 2017), all of which play essential roles in vertebrate forebrain development (Peng, 2006;Lagutin, 2003;Toresson et al;Kirkeby et al, 2012). While Gsx2 is also expressed in the pBV, this is only in later stages of development (tailbud stages).…”

Section: Posterior Brain Vesicle: Homology To the Midbrain?mentioning

confidence: 99%

Visual processing and fold-change detection by the larva of the simple chordateCiona

Smith

Borba

Schwennicke

et al. 2020

Preprint

View full text Add to dashboard Cite

SummaryVisuomotor inputs are processed to extract salient features. In vertebrates, the retina projects to processing centers in the midbrain optic tectum (OT; the superior colliculus in mammals) and the lateral geniculate nucleus, with the OT thought to be the more ancient [1]. The advent of the OT in chordates has been clouded by the reported absence of a midbrain homolog in the sister group to the vertebrates, the tunicates [2–7]. The best characterized tunicate nervous system is that of the Ciona larva, which, despite having only 177 central nervous system (CNS) neurons, has extensive homology with vertebrates CNSs [8,9]. Here we present anatomical, molecular, behavioral and connectomic data that the larval posterior brain vesicle (pBV) of Ciona shares homology with the vertebrate midbrain OT, suggesting their common ancestor possessed a tectum precursor. Moreover, we report that the conservation between the pBV and the OT extends to a role in visual processing. Ciona larvae have two distinct visuomotor behaviors – a looming shadow response and negative phototaxis [10]. These are mediated by separate neural pathways that initiate from different clusters of photoreceptors, both projecting to the pBV [11,12]. We report that inputs from both pathways are processed to generate fold-change detection (FCD) outputs [13]. However, the FCD responses differ between the two pathways, with the looming shadow response showing a power relationship to fold-change, while the navigation pathway responds linearly. Significantly, the connectivity and properties of pBV interneurons conform to known FCD circuit motifs, but with different circuit architectures for the two pathways. The negative phototaxis circuit forms an incoherent feedforward loop that involves interconnecting cholinergic and GABAergic interneurons. The looming shadow circuit uses the same cholinergic and GABAergic interneurons, but with different synaptic inputs to create a nonlinear integral feedback loop. These differing circuit architectures are reflected in the differing behavioral outputs.

show abstract

Patterning of brain precursors in ascidian embryos

Cited by 12 publications

References 49 publications

Fold Change Detection in Visual Processing

Fold Change Detection in Visual Processing

Onecut Regulates Core Components of the Molecular Machinery for Neurotransmission in Photoreceptor Differentiation

Visual processing and fold-change detection by the larva of the simple chordateCiona

Contact Info

Product

Resources

About