Complex schooling behaviors result from local interactions among individuals. Yet, how sensory signals from neighbors are analyzed in the visuomotor stream of animals is poorly understood. Here, we ...studied aggregation behavior in larval zebrafish and found that over development larvae transition from overdispersed groups to tight shoals. Using a virtual reality assay, we characterized the algorithms fish use to transform visual inputs from neighbors into movement decisions. We found that young larvae turn away from virtual neighbors by integrating and averaging retina-wide visual occupancy within each eye, and by using a winner-take-all strategy for binocular integration. As fish mature, their responses expand to include attraction to virtual neighbors, which is based on similar algorithms of visual integration. Using model simulations, we show that the observed algorithms accurately predict group structure over development. These findings allow us to make testable predictions regarding the neuronal circuits underlying collective behavior in zebrafish.
Visuomotor circuits filter visual information and determine whether or not to engage downstream motor modules to produce behavioral outputs. However, the circuit mechanisms that mediate and link ...perception of salient stimuli to execution of an adaptive response are poorly understood. We combined a virtual hunting assay for tethered larval zebrafish with two-photon functional calcium imaging to simultaneously monitor neuronal activity in the optic tectum during naturalistic behavior. Hunting responses showed mixed selectivity for combinations of visual features, specifically stimulus size, speed, and contrast polarity. We identified a subset of tectal neurons with similar highly selective tuning, which show non-linear mixed selectivity for visual features and are likely to mediate the perceptual recognition of prey. By comparing neural dynamics in the optic tectum during response versus non-response trials, we discovered premotor population activity that specifically preceded initiation of hunting behavior and exhibited anatomical localization that correlated with motor variables. In summary, the optic tectum contains non-linear mixed selectivity neurons that are likely to mediate reliable detection of ethologically relevant sensory stimuli. Recruitment of small tectal assemblies appears to link perception to action by providing the premotor commands that release hunting responses. These findings allow us to propose a model circuit for the visuomotor transformations underlying a natural behavior.
•Zebrafish hunting responses are triggered by conjunctions of visual features•Tectal neurons show non-linear mixed selectivity for prey-like visual stimuli•Tectal assemblies show premotor activity specifically preceding hunting responses
By combining a virtual hunting assay with functional calcium imaging, Bianco and Engert identify highly selective neurons in the zebrafish optic tectum that are likely to underlie visual prey recognition. The recruitment of tectal assemblies appears to link perception to action by providing the premotor commands that release hunting responses.
Larval zebrafish that are exposed repeatedly to dark looming stimuli will quickly habituate to these aversive signals and cease to respond with their stereotypical escape swims. A dark looming ...stimulus can be separated into two independent components: one that is characterized by an overall spatial expansion, where overall luminance is maintained at the same level, and a second, that represents an overall dimming within the whole visual field in the absence of any motion energy. Using specific stimulation patterns that isolate these independent components, we first extracted the behavioral algorithms that dictate how these separate information channels interact with each other and across the two eyes during the habituation process. Concurrent brain wide imaging experiments then permitted the construction of circuit models that suggest the existence of two separate neural pathways. The first is a looming channel which responds specifically to expanding edges presented to the contralateral eye and relays that information to the brain stem escape network to generate directed escapes. The second is a dimming-specific channel that could be either monocular or binocularly responsive, and that appears to specifically inhibit escape response when activated. We propose that this second channel is under strong contextual modulation and that it is primarily responsible for the incremental silencing of successive dark looming-evoked escapes.
Detailed descriptions of brain-scale sensorimotor circuits underlying vertebrate behavior remain elusive. Recent advances in zebrafish neuroscience offer new opportunities to dissect such circuits ...via whole-brain imaging, behavioral analysis, functional perturbations, and network modeling. Here, we harness these tools to generate a brain-scale circuit model of the optomotor response, an orienting behavior evoked by visual motion. We show that such motion is processed by diverse neural response types distributed across multiple brain regions. To transform sensory input into action, these regions sequentially integrate eye- and direction-specific sensory streams, refine representations via interhemispheric inhibition, and demix locomotor instructions to independently drive turning and forward swimming. While experiments revealed many neural response types throughout the brain, modeling identified the dimensions of functional connectivity most critical for the behavior. We thus reveal how distributed neurons collaborate to generate behavior and illustrate a paradigm for distilling functional circuit models from whole-brain data.
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•Optomotor response is driven asymmetrically by visual motion to each eye•Dedicated circuits differentially process eye- and direction-specific motion•Neural representations are distributed over select overrepresented response types•Behavior and neural activity are captured by realistic whole-brain circuit model
Whole-brain imaging and behavioral analysis combined with network modeling reveal key circuit elements contributing to a complex sensorimotor behavior in zebrafish larvae and provide a framework for building brain-level circuit models.
We review visually guided behaviors in larval zebrafish and summarise what is known about the neural processing that results in these behaviors, paying particular attention to the progress made in ...the last 2 years. Using the examples of the optokinetic reflex, the optomotor response, prey tracking and the visual startle response, we illustrate how the larval zebrafish presents us with a very promising model vertebrate system that allows neurocientists to integrate functional and behavioral studies and from which we can expect illuminating insights in the near future.
In the absence of salient sensory cues to guide behavior, animals must still execute sequences of motor actions in order to forage and explore. How such successive motor actions are coordinated to ...form global locomotion trajectories is unknown. We mapped the structure of larval zebrafish swim trajectories in homogeneous environments and found that trajectories were characterized by alternating sequences of repeated turns to the left and to the right. Using whole-brain light-sheet imaging, we identified activity relating to the behavior in specific neural populations that we termed the anterior rhombencephalic turning region (ARTR). ARTR perturbations biased swim direction and reduced the dependence of turn direction on turn history, indicating that the ARTR is part of a network generating the temporal correlations in turn direction. We also find suggestive evidence for ARTR mutual inhibition and ARTR projections to premotor neurons. Finally, simulations suggest the observed turn sequences may underlie efficient exploration of local environments.
Nervous systems have evolved to combine environmental information with internal state to select and generate adaptive behavioral sequences. To better understand these computations and their ...implementation in neural circuits, natural behavior must be carefully measured and quantified. Here, we collect high spatial resolution video of single zebrafish larvae swimming in a naturalistic environment and develop models of their action selection across exploration and hunting. Zebrafish larvae swim in punctuated bouts separated by longer periods of rest called interbout intervals. We take advantage of this structure by categorizing bouts into discrete types and representing their behavior as labeled sequences of bout types emitted over time. We then construct probabilistic models—specifically, marked renewal processes—to evaluate how bout types and interbout intervals are selected by the fish as a function of its internal hunger state, behavioral history, and the locations and properties of nearby prey. Finally, we evaluate the models by their predictive likelihood and their ability to generate realistic trajectories of virtual fish swimming through simulated environments. Our simulations capture multiple timescales of structure in larval zebrafish behavior and expose many ways in which hunger state influences their action selection to promote food seeking during hunger and safety during satiety.
•Naturalistic larval zebrafish behavior is observed with a moving camera system•Probabilistic models are used to predict and simulate behavioral sequences•Models combine environmental dynamics, behavioral history, and hunger state•Simulations capture behavioral dynamics spanning multiple timescales
Johnson et al. use a moving camera system to observe naturalistic larval zebrafish behavior and develop probabilistic models to predict and simulate behavioral sequences. Their simulations capture behavioral dynamics spanning multiple timescales, from reactions to prey to hunger-dependent changes in action selection across hunting and exploration.
Animal brains have evolved to encode social stimuli and transform these representations into advantageous behavioral responses. The commonalities and differences of these representations across ...species are not well-understood. Here, we show that social isolation activates an oxytocinergic (OXT), nociceptive circuit in the larval zebrafish hypothalamus and that chemical cues released from conspecific animals are potent modulators of this circuit's activity. We delineate an olfactory to subpallial pathway that transmits chemical social cues to OXT circuitry, where they are transformed into diverse outputs simultaneously regulating avoidance and feeding behaviors. Our data allow us to propose a model through which social stimuli are integrated within a fundamental neural circuit to mediate diverse adaptive behaviours.
Escape behaviors deliver organisms away from imminent catastrophe. Here, we characterize behavioral responses of freely swimming larval zebrafish to looming visual stimuli simulating predators. We ...report that the visual system alone can recruit lateralized, rapid escape motor programs, similar to those elicited by mechanosensory modalities. Two-photon calcium imaging of retino-recipient midbrain regions isolated the optic tectum as an important center processing looming stimuli, with ensemble activity encoding the critical image size determining escape latency. Furthermore, we describe activity in retinal ganglion cell terminals and superficial inhibitory interneurons in the tectum during looming and propose a model for how temporal dynamics in tectal periventricular neurons might arise from computations between these two fundamental constituents. Finally, laser ablations of hindbrain circuitry confirmed that visual and mechanosensory modalities share the same premotor output network. We establish a circuit for the processing of aversive stimuli in the context of an innate visual behavior.
•Larval zebrafish escape from looming stimuli after a critical image size is reached•Population activity of neurons in the optic tectum encodes critical image size•Modeling predicts the critical role of characterized cell types in the retina and tectum•Motor output is conveyed via multimodal circuitry in the hindbrain
Dunn et al. characterize the parameters influencing visually evoked escape behavior in larval zebrafish. Via large-scale functional imaging, the authors identify the neural circuits underlying the behavior and provide a mechanistic model that incorporates newly classified neural response types.
In order to localize the neural circuits involved in generating behaviors, it is necessary to assign activity onto anatomical maps of the nervous system. Using brain registration across hundreds of ...larval zebrafish, we have built an expandable open-source atlas containing molecular labels and definitions of anatomical regions, the Z-Brain. Using this platform and immunohistochemical detection of phosphorylated extracellular signal–regulated kinase (ERK) as a readout of neural activity, we have developed a system to create and contextualize whole-brain maps of stimulus- and behavior-dependent neural activity. This mitogen-activated protein kinase (MAP)-mapping assay is technically simple, and data analysis is completely automated. Because MAP-mapping is performed on freely swimming fish, it is applicable to studies of nearly any stimulus or behavior. Here we demonstrate our high-throughput approach using pharmacological, visual and noxious stimuli, as well as hunting and feeding. The resultant maps outline hundreds of areas associated with behaviors.
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