Prepontine non-giant neurons drive flexible escape behavior in zebrafish

Marquart, Gregory D.; Tabor, Kathryn M.; Bergeron, Sadie A.; Briggman, Kevin L.; Burgess, Harold A.

doi:10.1101/668517

Cited by 12 publications

(14 citation statements)

References 46 publications

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“…For example, in zebrafish, the balance of excitation between M-cells is controlled by feedforward inhibition from local neurons and this can contribute to the initial selection of which side is activated during escape (17,29). Modulator circuits in the brain also contribute to mediating a more flexible escape behavior (19,20,(64)(65)(66)(67)(68). Our results now demonstrate an additional layer of processing at the spinal cord level that not only transforms escape commands into motor action, but could provide an additional level of computation that could take into account spinal local inputs to determine the extent of the escape movement and control its trajectory.…”

Section: Discussionmentioning

confidence: 99%

A specialized spinal circuit for command amplification and directionality during escape behavior

Guan

Zhang

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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In vertebrates, action selection often involves higher cognition entailing an evaluative process. However, urgent tasks, such as defensive escape, require an immediate implementation of the directionality of escape trajectory, necessitating local circuits. Here we reveal a specialized spinal circuit for the execution of escape direction in adult zebrafish. A central component of this circuit is a unique class of segmentally repeating cholinergic V2a interneurons expressing the transcription factor Chx10. These interneurons amplify brainstem-initiated escape commands and rapidly deliver the excitation via a feedforward circuit to all fast motor neurons and commissural interneurons to direct the escape maneuver. The information transfer within this circuit relies on fast and reliable axo-axonic synaptic connections, bypassing soma and dendrites. Unilateral ablation of cholinergic V2a interneurons eliminated escape command propagation. Thus, in vertebrates, local spinal circuits can implement directionality of urgent motor actions vital for survival.

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Section: Discussionmentioning

confidence: 99%

A specialized spinal circuit for command amplification and directionality during escape behavior

Guan

Zhang

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…The mechanism allowing the modulation of Stage 1 turning angles in the 0 ms and 33 ms treatments could be related to the activity of Mauthner cells and associated neurons, as well as the prepontine neurons (Marquart et al, 2019). Prepontine neurons facilitate the integration of multiple sensory information (visual and auditory) and alter Stage 1 of the escape response (Marquart et al, 2019). It is possible that a similar mechanism may occur in the presence of two visual stimuli; i.e.…”

Section: Discussionmentioning

confidence: 99%

“…a ballistic response) (Sato et al, 2019). In fish, recent work has shown that larval zebrafish may be able to integrate sensory information from multiple threats during delayed escape responses due to a cluster of 38 prepontine neurons that are not part of the fast escape neural pathway (Marquart et al, 2019). This finding suggests that during the initial escape latency (i.e.…”

Section: Introductionmentioning

confidence: 99%

Escaping from multiple visual threats: Modulation of escape responses in Pacific staghorn sculpin (Leptocottus armatus)

Kimura

Pfalzgraff

Levet

et al. 2021

Preprint

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Fish perform rapid escape responses to avoid sudden predatory attacks. During escape responses, fish bend their bodies into a C-shape and quickly turn away from the predator and accelerate. The escape trajectory is determined by the initial turn (Stage 1) and a contralateral bend (Stage 2). Previous studies have used a single threat or model predator as a stimulus. In nature, however, multiple predators may attack from different directions simultaneously or in close succession. It is unknown whether fish are able to change the course of their escape response when startled by multiple stimuli at various time intervals. Pacific staghorn sculpin (Leptocottus armatus) were startled with a left and right visual stimulus in close succession. By varying the timing of the second stimulus, we were able to determine when and how a second stimulus could affect the escape response direction. Four treatments were used: a single visual stimulus (control); or two stimuli coming from opposite sides separated by a 0 ms (simultaneous treatment); a 33 ms; or a 83 ms time interval. The 33 ms and 83 ms time intervals were chosen to occur shortly before and after a predicted 60 ms visual escape latency (i.e. during Stage 1). The 0 ms and 33 ms treatments influenced both the escape trajectory and the Stage 1 turning angle, compared to a single stimulation, whereas the 83 ms treatment had no effect on the escape response. We conclude that Pacific staghorn sculpin can modulate their escape response only between stimulation and the onset of the response, but that escape responses are ballistic after the body motion has started.

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“…No other binary or three component mixture induced statistically significant effects compare to controls. We also analyzed the frequency of long latency C-bends (LLCs), which are normal responses typically elicited by weaker stimuli and that are independent of the Mauthner cell and instead rely on the activation of prepontine neurons (Marquart et al 2019).…”

Section: 3mentioning

confidence: 99%

The cyanotoxin 2,4-DAB enhances mortality and causes behavioral and molecular dysfunctions associated with neurodegeneration in larval zebrafish

Martin

Bereman

Marsden

2021

Preprint

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Exposure to cyanotoxins has been linked to neurodegenerative diseases, including amyotrophic lateral sclerosis, Alzheimer's, and Parkinson's disease. While the cyanotoxin beta-methylamino-L-alanine (BMAA) has received much attention, cyanobacteria produce many cyanotoxic compounds, several of which have been detected in nature alongside BMAA including 2,4-diaminobutyric acid (2,4-DAB), and N-(2-aminoethyl)glycine (AEG). Thus, the question of whether DAB and AEG also cause neurotoxic effects in vivo is of great interest, as is the question of whether they interact to enhance toxicity. Here, we evaluate the toxic and neurotoxic effects of these cyanotoxins alone or in combination by measuring zebrafish larval viability and behavior after exposure. 2,4-DAB was the most potent cyanotoxin as it decreased larval viability by approximately 50% at 6 days post fertilization, while BMAA and AEG decreased viability by just 16% and 8%, respectively. Although we only observed minor neurotoxic effects on spontaneous locomotion, BMAA and AEG enhanced acoustic startle sensitivity, and they interacted in an additive manner to exert their effects. 2,4-DAB, however, only modulated the startle kinematics, an indication of motor dysfunction. To investigate the mechanisms of 2,4-DAB's effects, we analyzed the protein profile of larval zebrafish exposed to 500 uM 2,4-DAB at two time points and identified molecular signatures consistent with neurodegeneration, including disruption of metabolic pathways and downregulation of the ALS-associated genes SOD1 and UBQLN4. Together, our data demonstrate that BMAA and its isomers AEG and 2,4-DAB cause neurotoxic effects in vivo, with 2,4-DAB as the most potent of the three in the zebrafish model.

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Prepontine non-giant neurons drive flexible escape behavior in zebrafish

Cited by 12 publications

References 46 publications

A specialized spinal circuit for command amplification and directionality during escape behavior

A specialized spinal circuit for command amplification and directionality during escape behavior

Escaping from multiple visual threats: Modulation of escape responses in Pacific staghorn sculpin (Leptocottus armatus)

The cyanotoxin 2,4-DAB enhances mortality and causes behavioral and molecular dysfunctions associated with neurodegeneration in larval zebrafish

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