A circuit motif in the zebrafish hindbrain for a two alternative behavioral choice to turn left or right

Koyama, Minoru; Minale, Francesca; Shum, Jennifer; Nishimura, Nozomi; Schaffer, Chris B.; Fetcho, Joseph R.

doi:10.7554/elife.16808

Cited by 73 publications

(67 citation statements)

References 46 publications

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“…This necessitates a means of directional coding [38]. Our work suggests variations in escape trajectory can be explained largely by the duration of the initial bend, and to a lesser extent by tail angle velocity.…”

Section: Discussionmentioning

confidence: 99%

Visual Threat Assessment and Reticulospinal Encoding of Calibrated Responses in Larval Zebrafish

2017

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Summary All visual animals must decide whether approaching objects are a threat. Our current understanding of this process has identified a proximity-based mechanism where an evasive maneuver is triggered when a looming stimulus passes a subtended visual angle threshold. However, some escape strategies are more costly than others and so it would be beneficial to additionally encode the level of threat conveyed by the predator's approach rate to select the most appropriate response. Here, using naturalistic rates of looming visual stimuli while simultaneously monitoring escape behavior and the recruitment of multiple reticulospinal neurons, we find that larval zebrafish do indeed perform a calibrated assessment of threat. While all fish generate evasive maneuvers at the same subtended visual angle, lower approach rates evoke slower, more kinematically variable escape responses with relatively long latencies as well as the unilateral recruitment of ventral spinal projecting nuclei (vSPNs) implicated in turning. In contrast, higher approach rates evoke faster, more kinematically stereotyped responses with relatively short latencies, as well as bilateral recruitment of vSPNs and unilateral recruitment of giant fiber neurons in fish and amphibians called Mauthner cells. In addition to the higher proportion of more costly, shorter latency Mauthner-active responses to greater perceived threats, we observe a higher incidence of freezing behavior at higher approach rates. Our results provide a new framework to understand how behavioral flexibility is grounded in the appropriate balancing of trade-offs between fast and slow movements when deciding to respond to a visually perceived threat.

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Section: Discussionmentioning

confidence: 99%

Visual Threat Assessment and Reticulospinal Encoding of Calibrated Responses in Larval Zebrafish

2017

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“…Recording was delayed by about 50 minutes (on average) relative to recordings without laser ablation. We performed axotomies using an apparatus pioneered by Tsai et al (2009) and optimized by Koyama et al (2016). We used a high-power (8W) fixed wavelength (1040 nm) low-repetition rate (200 kHz) pulsed infrared laser (305 fs) with integrated pulse picker (Spirit One, Spectra-Physics).…”

Section: -Photon Laser Ablationmentioning

confidence: 99%

Encoding of wind direction by central neurons inDrosophila

Suver

Matheson

Sarkar

et al. 2018

Preprint

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Wind is a major navigational cue for insects, but how wind direction is decoded by central neurons in the insect brain is unknown. Here, we find that walking flies combine signals from both antennae to orient to wind during olfactory search behavior. Movements of single antennae are ambiguous with respect to wind direction, but the difference between left and right antennal displacements yields a linear code for wind direction in azimuth. Second-order mechanosensory neurons share the ambiguous responses of single antenna and receive input primarily from the ipsilateral antenna.Finally, we identify a novel set of neurons, which we call wedge projection neurons, that integrate signals across the two antennae and receive input from at least three classes of second-order neurons to produce a more linear representation of wind direction. This study establishes how a feature of the sensory environment -the wind direction -is decoded by single neurons that compare information across two sensors.

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“…A third difference is the mechanism for selecting escape direction. Feed-forward inhibitory signals help to select activation of a single M-cell (Koyama et al, 2016); however acoustic stimuli often activate both M-cells and downstream mechanisms prevent simultaneous bilateral activation of motor pools (Satou et al, 2009). In contrast, prepontine neurons show much greater activity on the side ipsilateral to the escape direction.…”

Section: Discussionmentioning

confidence: 99%

“…Central to the escape circuit are the Mauthner cells, a bilateral pair of giant reticulospinal neurons that trigger explosive C-start maneuvers with a single action potential (Eaton et al, 1981(Eaton et al, , 1977bZottoli, 1977). However, a second class of escape swim has also been described (Burgess and Granato, 2007;Eaton et al, 1977aEaton et al, , 1982Koyama et al, 2016). Zebrafish larvae respond to auditory stimuli with kinematically distinct short-latency C-starts (SLCs) and long-latency C-starts (LLCs) (Burgess and Granato, 2007;Issa et al, 2011;Jain et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Prepontine non-giant neurons drive flexible escape behavior in zebrafish

Marquart

Tabor

Bergeron

et al. 2019

Preprint

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Many species execute ballistic escape reactions to avoid imminent danger. Despite fast reaction times, responses are often highly regulated, reflecting a trade-off between costly motor actions and perceived threat level. However, how sensory cues are integrated within premotor escape circuits remains poorly understood. Here we show that in zebrafish, less precipitous threats elicit a delayed escape, characterized by flexible trajectories, that are driven by a cluster of 38 prepontine neurons that are completely separate from the fast escape pathway. Whereas neurons that initiate rapid escapes receive direct auditory input and drive motor neurons, input and output pathways for delayed escapes are indirect, facilitating integration of cross-modal sensory information. Rapid decision making in the escape system is thus enabled by parallel pathways for ballistic responses and flexible delayed actions.

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A circuit motif in the zebrafish hindbrain for a two alternative behavioral choice to turn left or right

Cited by 73 publications

References 46 publications

Visual Threat Assessment and Reticulospinal Encoding of Calibrated Responses in Larval Zebrafish

Visual Threat Assessment and Reticulospinal Encoding of Calibrated Responses in Larval Zebrafish

Encoding of wind direction by central neurons inDrosophila

Prepontine non-giant neurons drive flexible escape behavior in zebrafish

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