Whole-field Visual Motion Drives Swimming in Larval Zebrafish Via a Stochastic Process

Overview

Journal J Exp Biol

Specialty Biology

Date 2015 Mar 21

PMID 25792753

Citations 13

Authors

Ruben Portugues

Martin Haesemeyer

Mirella L Blum

Florian Engert

Affiliations

Soon will be listed here.

Abstract

Caudo-rostral whole-field visual motion elicits forward locomotion in many organisms, including larval zebrafish. Here, we investigate the dependence on the latency to initiate this forward swimming as a function of the speed of the visual motion. We show that latency is highly dependent on speed for slow speeds (<10 mm s(-1)) and then plateaus for higher values. Typical latencies are >1.5 s, which is much longer than neuronal transduction processes. What mechanisms underlie these long latencies? We propose two alternative, biologically inspired models that could account for this latency to initiate swimming: an integrate and fire model, which is history dependent, and a stochastic Poisson model, which has no history dependence. We use these models to predict the behavior of larvae when presented with whole-field motion of varying speed and find that the stochastic process shows better agreement with the experimental data. Finally, we discuss possible neuronal implementations of these models.

Citing Articles

Predictive neural computations in the cerebellum contribute to motor planning and faster behavioral responses in larval zebrafish.

Narayanan S, Varma A, Thirumalai V Sci Adv. 2024; 10(1):eadi6470.

PMID: 38170763 PMC: 10775999. DOI: 10.1126/sciadv.adi6470.

Dimensionality reduction reveals separate translation and rotation populations in the zebrafish hindbrain.

Feierstein C, de Goeij M, Ostrovsky A, Laborde A, Portugues R, Orger M Curr Biol. 2023; 33(18):3911-3925.e6.

PMID: 37689065 PMC: 10524920. DOI: 10.1016/j.cub.2023.08.037.

A behavioral and modeling study of control algorithms underlying the translational optomotor response in larval zebrafish with implications for neural circuit function.

Holman J, Lai W, Pichler P, Saska D, Lagnado L, Buckley C PLoS Comput Biol. 2023; 19(2):e1010924.

PMID: 36821587 PMC: 9998047. DOI: 10.1371/journal.pcbi.1010924.

Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae.

Lagogiannis K, Diana G, Meyer M Elife. 2020; 9.

PMID: 32773042 PMC: 7561354. DOI: 10.7554/eLife.55119.

Development of a larval fathead minnow optomotor response assay for assessing visual function.

Krzykwa J, Jeffries M MethodsX. 2020; 7:100971.

PMID: 32642453 PMC: 7334461. DOI: 10.1016/j.mex.2020.100971.

References

Gerstein G, Mandelbrot B . RANDOM WALK MODELS FOR THE SPIKE ACTIVITY OF A SINGLE NEURON. Biophys J. 1964; 4:41-68. PMC: 1367440. DOI: 10.1016/s0006-3495(64)86768-0. View

Severi K, Portugues R, Marques J, OMalley D, Orger M, Engert F . Neural control and modulation of swimming speed in the larval zebrafish. Neuron. 2014; 83(3):692-707. PMC: 4126853. DOI: 10.1016/j.neuron.2014.06.032. View

Shadlen M, Newsome W . Noise, neural codes and cortical organization. Curr Opin Neurobiol. 1994; 4(4):569-79. DOI: 10.1016/0959-4388(94)90059-0. View

Korn H, Faber D . The Mauthner cell half a century later: a neurobiological model for decision-making?. Neuron. 2005; 47(1):13-28. DOI: 10.1016/j.neuron.2005.05.019. View

Khater T, Quinn K, Pena J, Baker J, Peterson B . The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation. Exp Brain Res. 1993; 94(1):16-32. DOI: 10.1007/BF00230467. View

Hanes D, Schall J . Neural control of voluntary movement initiation. Science. 1996; 274(5286):427-30. DOI: 10.1126/science.274.5286.427. View

SHIK M, Severin F, Orlovsky G . Control of walking and running by means of electrical stimulation of the mesencephalon. Electroencephalogr Clin Neurophysiol. 1969; 26(5):549. View

Fry S, Rohrseitz N, Straw A, Dickinson M . Visual control of flight speed in Drosophila melanogaster. J Exp Biol. 2009; 212(Pt 8):1120-30. DOI: 10.1242/jeb.020768. View

Orger M, Kampff A, Severi K, Bollmann J, Engert F . Control of visually guided behavior by distinct populations of spinal projection neurons. Nat Neurosci. 2008; 11(3):327-33. PMC: 2894808. DOI: 10.1038/nn2048. View

10.

Portugues R, Engert F . Adaptive locomotor behavior in larval zebrafish. Front Syst Neurosci. 2011; 5:72. PMC: 3163830. DOI: 10.3389/fnsys.2011.00072. View

11.

Burkitt A . A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input. Biol Cybern. 2006; 95(1):1-19. DOI: 10.1007/s00422-006-0068-6. View

12.

David C . Optomotor control of speed and height by free-flying Drosophila. J Exp Biol. 1979; 82:389-92. DOI: 10.1242/jeb.82.1.389. View

13.

Robinson D . Integrating with neurons. Annu Rev Neurosci. 1989; 12:33-45. DOI: 10.1146/annurev.ne.12.030189.000341. View

14.

Dieringer N, Precht W . Compensatory head and eye movements in the frog and their contribution to stabilization of gaze. Exp Brain Res. 1982; 47(3):394-406. DOI: 10.1007/BF00239357. View

15.

Shadlen M, Newsome W . The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci. 1998; 18(10):3870-96. PMC: 6793166. View

16.

Srinivasan M, Poteser M, Kral K . Motion detection in insect orientation and navigation. Vision Res. 1999; 39(16):2749-66. DOI: 10.1016/s0042-6989(99)00002-4. View

17.

Stevens C, Zador A . Input synchrony and the irregular firing of cortical neurons. Nat Neurosci. 1999; 1(3):210-7. DOI: 10.1038/659. View

18.

Schall J, Thompson K . Neural selection and control of visually guided eye movements. Annu Rev Neurosci. 1999; 22:241-59. DOI: 10.1146/annurev.neuro.22.1.241. View

19.

Portugues R, Engert F . The neural basis of visual behaviors in the larval zebrafish. Curr Opin Neurobiol. 2009; 19(6):644-7. PMC: 4524571. DOI: 10.1016/j.conb.2009.10.007. View

20.

van Vreeswijk C, Sompolinsky H . Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science. 1996; 274(5293):1724-6. DOI: 10.1126/science.274.5293.1724. View