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Modeling the Neural Control of Zebrafish Locomotive Behaviors
Scott A. Hill, Xiao-Ping Liu, Melissa A. Borla, Jorge V. José, and Donald M. O'Malley

Departments of Physics and Biology, and the
Center for Interdisciplinary Research in Complex Systems (CIRCS)
Northeastern University, Boston MA


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Movies of larval zebrafish

A larva performing a slow swim

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A larva capturing a paramecium

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What we are trying to do
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Poster presented at Neuroscience 2003,
the Society for Neuroscience's annual meeting

Larval zebrafish exhibit a sophisticated locomotive repertoire which depends on neural control signals that descend from brainstem to spinal cord (Budick and O'Malley, 2000; Borla et al., 2002). Because of the complexity of the descending motor control system in brainstem (O'Malley et al., 2003) and the complexity of the spinal networks that receive and respond to descending signals (Hale et al., 2001), it is difficult to learn the nature of the controls that shape larval locomotive behaviors (which include: routine turns, escape behaviors, prey-tracking and prey capture). We have therefore turned to modeling of both the kinematics of the animal's behaviors and the underlying neural networks. Our goal is to understand how the complex locomotive maneuvers exhibited by these larvae are generated.

The functioning of spinal networks that underlie locomotion in fishes and tadpoles has been extensively modeled (see e.g. Roberts and Tunstall, 1990; Dale, 1995; Grillner, 2003; Dale, 2003). While swimming in lamprey has been well studied, swimming in Xenopus tadpoles may better match larval zebrafish swimming, in terms of body form and locomotive repertoire. We therefore created a model based on Xenopus spinal network models that incorporate known properties of the oscillators underlying swimming (Tunstall et al. 2002). We first explored the control of tail-beat frequency (TBF), and found that by altering the synaptic strengths of AMPA, NMDA and Glycinergic-like synapses (all known to be present in Xenopus spinal cord), we were able to generate TBFs that spanned the range of speeds observed during burst and slow swimming behaviors. We then extended this to a multi-segment model. While regular rhythmic patterns could be generated, several marked deviations from an idealized undulatory behavior were observed. We also created a simple mechanical or "kinematic" model to visualize how network activity might be transformed into larval behaviors. This kinematic model could be driven by either neural network activity or alternatively by a set of descending control parameters.


Simulating a slow swim
Modelling a slow swim, using simulated descending control
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Modelling a slow swim using output from simulated neurons (using NEURON).
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J-bend

A zebrafish performing a J-bend during a capture swim.

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Simulation of a J-bend, implemented using a combination of an oscillatory burst pattern (just as in the swimming motion above), a tonic bending signal, and an inhibitory "stiffening" signal sent to the rostral portion of the fish.
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Varying the stiffness of the spine

In our original simulations, we assumed that all segments of the fish responded identically to descending controls, as if the fish were cylindrical.
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However, we get a more realistic motion if we assume that the tail of the fish is more flexible than the head. Mathematically speaking, we say that the curvature of a segment is proportional not just to the signal received from the spinal cord, but also inversely proportional to the width parameter W(x), where W(x) is chosen to be roughly linear.
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Here is a picture of an actual zebrafish for comparison.
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