Antagonistic Inhibitory Circuits Integrate Visual and Gravitactic Behaviors

Bostwick, Michaela; Smith, Eleanor L.; Borba, Cezar; Newman-Smith, Erin; Guleria, Iraa; Kourakis, Matthew J.; Smith, William C.

doi:10.1016/j.cub.2019.12.017

Cited by 31 publications

(48 citation statements)

References 46 publications

(78 reference statements)

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“…To assess the behavior of larvae, we used a previously described gravitaxis assay [ 8 ]. In this assay, the behavior of larvae is recorded in a vertically mounted and covered 6-cm petri dish.…”

Section: Resultsmentioning

confidence: 99%

“…For these assays presented here, which consisted of dimming a 505-nm light from 600 to 0 lux (while recording with constant 700-nm illumination), we recorded both the percentage of larvae responding to the dim, which was evident in recordings as swimming behavior initiated immediately following the light dim, as well as the direction of swim trajectories with respect to gravity for those larvae that did respond. All behavior assays were analyzed as described [ 8 ] and see the “ Methods ” section]. Briefly, trajectories were determined by assessing the starting and ending positions in the 20 s following dimming.…”

Section: Resultsmentioning

confidence: 99%

“…Yet, the simple CNS of the swimming tadpole larva of the tunicate Ciona contains less than 200 neurons, a vast contrast to cell numbers in the millions or even billions for their nearest chordate relatives, the vertebrates [ 6 ]. With an electron-micrograph-derived synaptic connectome [ 7 ], and a range of quantifiable behaviors [ 8 , 9 ], the Ciona CNS is fertile ground for researchers seeking to bridge neural circuitry and behavior. Studies have begun to shed light on the circuit logic which governs larval behaviors.…”

Section: Introductionmentioning

confidence: 99%

“…The antenna cells (Fig. 1 ) sense the movement of the otolith pigment cell as the larva moves with respect to gravity, but the targets of the antenna cell in the pBV, the antenna relay neurons , are inhibited by photoreceptor RNs, unless the larva sees a light dim, at which point the inhibition is released and the larva swims upwards [ 8 ].

Fig.…”

Section: Introductionmentioning

confidence: 99%

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Disruption of left-right axis specification in Ciona induces molecular, cellular, and functional defects in asymmetric brain structures

Kourakis

Bostwick

et al. 2021

BMC Biol

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Background Left-right asymmetries are a common feature of metazoans and can be found in a number of organs including the nervous system. These asymmetries are particularly pronounced in the simple central nervous system (CNS) of the swimming tadpole larva of the tunicate Ciona, which displays a chordate ground plan. While common pathway elements for specifying the left/right axis are found among chordates, particularly a requirement for Nodal signaling, Ciona differs temporally from its vertebrate cousins by specifying its axis at the neurula stage, rather than at gastrula. Additionally, Ciona and other ascidians require an intact chorionic membrane for proper left-right specification. Whether such differences underlie distinct specification mechanisms between tunicates and vertebrates will require broad understanding of their influence on CNS formation. Here, we explore the consequences of disrupting left-right axis specification on Ciona larval CNS cellular anatomy, gene expression, synaptic connectivity, and behavior. Results We show 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 projections, 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. Conclusions 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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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Fig.…”

Section: Introductionmentioning

confidence: 99%

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Disruption of left-right axis specification in Ciona induces molecular, cellular, and functional defects in asymmetric brain structures

Kourakis

Bostwick

et al. 2021

BMC Biol

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“…More recently, a larval nervous system connectome has been revealed [ 28 ] and collections of single cell transcriptomics generated [ 29 , 30 , 31 , 32 , 33 ]. Emerging studies are now aiming to annotate each neuron identified in the connectome with the gene expression patterns, including neurotransmitter types, described from in situ hybridization/immunostaining analysis or single cell transcriptomics datasets, as well as to the cell lineage history and ultimately to neuronal function and larval behavior [ 29 , 34 , 35 , 36 , 37 , 38 , 39 ].…”

Section: The Ascidian Larval Cnsmentioning

confidence: 99%

Neuromesodermal Lineage Contribution to CNS Development in Invertebrate and Vertebrate Chordates

Hudson

Yasuo

2021

Genes

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Ascidians are invertebrate chordates and the closest living relative to vertebrates. In ascidian embryos a large part of the central nervous system arises from cells associated with mesoderm rather than ectoderm lineages. This seems at odds with the traditional view of vertebrate nervous system development which was thought to be induced from ectoderm cells, initially with anterior character and later transformed by posteriorizing signals, to generate the entire anterior-posterior axis of the central nervous system. Recent advances in vertebrate developmental biology, however, show that much of the posterior central nervous system, or spinal cord, in fact arises from cells that share a common origin with mesoderm. This indicates a conserved role for bi-potential neuromesoderm precursors in chordate CNS formation. However, the boundary between neural tissue arising from these distinct neural lineages does not appear to be fixed, which leads to the notion that anterior-posterior patterning and neural fate formation can evolve independently.

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Collective Behaviors of Active Matter Learning from Natural Taxes Across Scales

Pumera

et al. 2022

Advanced Materials

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Figure 1. Cognate collective taxis behaviors realized by organisms and robots across scales. A) Collective migration of particle robots and cells. Loosely coupled particles present collective phototaxis (left). Reproduced with permission. [11] Copyright 2019, Springer Nature. Cells perform collective migration in 3D environments (right). Reproduced with permission. [4] Copyright 2018, Springer Nature. B) Self-assembly of robots and bacteria. A swarm of 1024 kilobots form a star-like pattern (left). Reproduced with permission. [14] Copyright 2014, AAAS. A swarm of E. coli cells form a right-handed colony (right). Scale bar: 5 mm. Reproduced with permission. [15] Copyright 2011, The Proceedings of the National Academy of Sciences. C) Collective taxes of macroscopic organisms (e.g., fishes, birds, and ants) and robots. D) Collective taxes of microorganisms (e.g., sperms, [19] cells, and bacteria [20] ) and microrobots. [21] E) Connection constructed by ants and NPs. Weaver ants establish a bridge to connect leaves (left). Reproduced with permission. [7] Copyright 2002, Springer Nature. Magnetic NPs with gold functionalization connect two broken electrodes in a targeted position (right). Reproduced with permission. [16] Copyright 2019, American Chemical Society. F) Avoidance of predators. A bait ball of fishes is formed during the hunting of a sea lion (left). Reproduced with permission. [22] Copyright 2019, Science and Information Organization. The biomimetic predator-prey behavior in a binary system of active micromotors (right). Reproduced with permission. [17] Copyright 2019, American Chemical Society.

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Antagonistic Inhibitory Circuits Integrate Visual and Gravitactic Behaviors

Cited by 31 publications

References 46 publications

Disruption of left-right axis specification in Ciona induces molecular, cellular, and functional defects in asymmetric brain structures

Disruption of left-right axis specification in Ciona induces molecular, cellular, and functional defects in asymmetric brain structures

Neuromesodermal Lineage Contribution to CNS Development in Invertebrate and Vertebrate Chordates

Collective Behaviors of Active Matter Learning from Natural Taxes Across Scales

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