Antagonistic Inhibitory Circuits Integrate Gravitactic and Visual Behaviors

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

doi:10.2139/ssrn.3482151

Cited by 6 publications

(23 citation statements)

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“…Thus both by gene expression and connectivity, the pBV shares many of the attributes of the vertebrate midbrain. The results presented here, and those recently published (Bostwick et al, 2020), indicate that the pBV does not simply relay sensory input to the MG, but rather plays a role in sensory processing and integration. Thus, we can add to the list of similarities between the pBV and the midbrain an apparent conservation of function.…”

Section: Discussionsupporting

confidence: 76%

“…Several lines of evidence, both published and newly presented here, point to the importance of the pBV in processing visual input. For example, recently published work from our group details the convergence and integration of gravitaxis and visual inputs in the pBV (Bostwick et al, 2020). This multisensory pBV circuit suppresses gravitaxis behavior under constant light conductions, but releases this inhibition in response to dimming.…”

Section: Discussionmentioning

confidence: 99%

“…A fundamental property of FCD is that increases in the fold-change of a stimulus give an increased output, while the same fold-change, but of different absolute values, gives the same output. To investigate Ciona photoresponses, 25-hour post-fertilization larvae were first exposed to a fold-change dimming series using a 505 nm LED lamp while recording at far-red (700 nm), as described previously (Bostwick et al, 2020;Kourakis et al, 2019). The series ranged from 3-fold (600 lux to 200 lux) to 60-fold (600 lux to 10 lux) dimming ( Figure 1A and SFigure 1).…”

Section: Fold-change Transformation Of Visual Inputmentioning

confidence: 99%

“…The PR-Is are almost exclusively glutamatergic, and pharmacologic studies confirm that they relay to the MG via the cholinergic prRNs (Kourakis et al, 2019). By contrast, the PR-II circuit is more complex, and a combination of neurotransmitter use, pharmacological and mutant analyses strongly indicates that this pathway activates the MG via disinhibition (Bostwick et al, 2020;Kourakis et al, 2019). When we simplify the PR-I and PR-II circuits by combining cell types and synaptic connections we see the emergence of two likely FCD circuits ( Figure 3B).…”

Section: Putative Fold-change Detection Circuits In the Posterior Bramentioning

confidence: 99%

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

Smith

Borba

Schwennicke

et al. 2020

Preprint

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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.

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Section: Discussionsupporting

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Section: Fold-change Transformation Of Visual Inputmentioning

confidence: 99%

Section: Putative Fold-change Detection Circuits In the Posterior Bramentioning

confidence: 99%

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

Smith

Borba

Schwennicke

et al. 2020

Preprint

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“…Gravity is known as a critical factor to affect the function of cognition as well as behaviors [1][2][3]. The altered gravity was mainly detected in the peripheral vestibular system, especially otolith, and the corresponding neural information is sent to the central nervous system [4,5]. Initially, the changed gravity affects the membrane viscosity, which decreases or increases under hypo-or hypergravity, respectively [6].…”

Section: Introductionmentioning

confidence: 99%

Vestibular Responses to Gravity Alterations

Nguyen¹,

Kim²,

Kim³

2020

Res Vestib Sci

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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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Antagonistic Inhibitory Circuits Integrate Gravitactic and Visual Behaviors

Cited by 6 publications

References 0 publications

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

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

Vestibular Responses to Gravity Alterations

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

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