Elements of a stochastic 3D prediction engine in larval zebrafish prey capture
- Harvard University, United States
- Massachusetts Institute of Technology, United States
Abstract
The computational principles underlying predictive capabilities in animals are poorly understood. Here, we wondered whether predictive models mediating prey capture could be reduced to a simple set of sensorimotor rules performed by a primitive organism. For this task, we chose the larval zebrafish, a tractable vertebrate that pursues and captures swimming microbes. Using a novel naturalistic 3D setup, we show that the zebrafish combines position and velocity perception to construct a future positional estimate of its prey, indicating an ability to project trajectories forward in time. Importantly, the stochasticity in the fish's sensorimotor transformations provides a considerable advantage over equivalent noise-free strategies. This surprising result coalesces with recent findings that illustrate the benefits of biological stochasticity to adaptive behavior. In sum, our study reveals that zebrafish are equipped with a recursive prey capture algorithm, built up from simple stochastic rules, that embodies an implicit predictive model of the world.
Data availability
All software related to behavioral analysis, modeling, and virtual prey capture simulation is freely available at www.github.com/larrylegend33/PreycapMaster. The software is licensed under a GNU General Public License 3.0. Source data for analysis and simulations is enclosed as "Source Data" in relevant figures. Source Data for Figure 2 contains all pursuit bouts analyzed in the dataset; it was used to construct Figures 2, 3, 5, and 6A, and is accompanied by instructions for running queries. Source Data for Figure 6 contains the generators for simulating from the DPMMs in Figure 6. Using the code at www.github.com/larrylegend33/PreycapMaster and the generators in Source Data - Figure 6 requires obtaining the BayesDB software package, which is freely available at http://probcomp.csail.mit.edu/software/bayesdb/.
Article and author information
Author details
Funding
National Institutes of Health (U19NS104653)
- Florian Engert
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Experiments were conducted according to the guidelines of the National Institutes of Health and were approved by the Standing Committee on the Use of Animals in Research of Harvard University. Animals were handled according IACUC protocol #2729.
Copyright
© 2019, Bolton et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Elements of a stochastic 3D prediction engine in larval zebrafish prey capture
eLife 8:e51975.
https://doi.org/10.7554/eLife.51975
Further reading
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Transcranial ultrasonic stimulation (TUS) is rapidly emerging as a promising non-invasive neuromodulation technique. TUS is already well-established in animal models, providing foundations to now optimize neuromodulatory efficacy for human applications. Across multiple studies, one promising protocol, pulsed at 1000 Hz, has consistently resulted in motor cortical inhibition in humans (Fomenko et al., 2020). At the same time, a parallel research line has highlighted the potentially confounding influence of peripheral auditory stimulation arising from TUS pulsing at audible frequencies. In this study, we disentangle direct neuromodulatory and indirect auditory contributions to motor inhibitory effects of TUS. To this end, we include tightly matched control conditions across four experiments, one preregistered, conducted independently at three institutions. We employed a combined transcranial ultrasonic and magnetic stimulation paradigm, where TMS-elicited motor-evoked potentials (MEPs) served as an index of corticospinal excitability. First, we replicated motor inhibitory effects of TUS but showed through both tight controls and manipulation of stimulation intensity, duration, and auditory masking conditions that this inhibition was driven by peripheral auditory stimulation, not direct neuromodulation. Furthermore, we consider neuromodulation beyond driving overall excitation/inhibition and show preliminary evidence of how TUS might interact with ongoing neural dynamics instead. Primarily, this study highlights the substantial shortcomings in accounting for the auditory confound in prior TUS-TMS work where only a flip-over sham and no active control was used. The field must critically reevaluate previous findings given the demonstrated impact of peripheral confounds. Furthermore, rigorous experimental design via (in)active control conditions is required to make substantiated claims in future TUS studies. Only when direct effects are disentangled from those driven by peripheral confounds can TUS fully realize its potential for research and clinical applications.
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Background:
The dichotomy between the hypo- versus hyperkinetic nature of Parkinson’s disease (PD) and dystonia, respectively, is thought to be reflected in the underlying basal ganglia pathophysiology. In this study, we investigated differences in globus pallidus internus (GPi) neuronal activity, and short- and long-term plasticity of direct pathway projections.
Methods:
Using microelectrode recording data collected from the GPi during deep brain stimulation surgery, we compared neuronal spiketrain features between people with PD and those with dystonia, as well as correlated neuronal features with respective clinical scores. Additionally, we characterized and compared readouts of short- and long-term synaptic plasticity using measures of inhibitory evoked field potentials.
Results:
GPi neurons were slower, bustier, and less regular in dystonia. In PD, symptom severity positively correlated with the power of low-beta frequency spiketrain oscillations. In dystonia, symptom severity negatively correlated with firing rate and positively correlated with neuronal variability and the power of theta frequency spiketrain oscillations. Dystonia was moreover associated with less long-term plasticity and slower synaptic depression.
Conclusions:
We substantiated claims of hyper- versus hypofunctional GPi output in PD versus dystonia, and provided cellular-level validation of the pathological nature of theta and low-beta oscillations in respective disorders. Such circuit changes may be underlain by disease-related differences in plasticity of striato-pallidal synapses.
Funding:
This project was made possible with the financial support of Health Canada through the Canada Brain Research Fund, an innovative partnership between the Government of Canada (through Health Canada) and Brain Canada, and of the Azrieli Foundation (LM), as well as a grant from the Banting Research Foundation in partnership with the Dystonia Medical Research Foundation (LM).
