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Approaching object acceleration differentially affects the predictions of neuronal collision avoidance models

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Abstract

The processing of visual information for collision avoidance has been investigated at the biophysical level in several model systems. In grasshoppers, the (so-called) \(\eta \) model captures reasonably well the visual processing performed by an identified neuron called the lobular giant movement detector as it tracks approaching objects. Similar phenomenological models have been used to describe either the firing rate or the membrane potential of neurons responsible for visually guided collision avoidance in other animals. Specifically, in goldfish, the \(\kappa \) model has been proposed to describe the Mauthner cell, an identified neuron involved in startle escape responses. In the vinegar fly, a third model was developed for the giant fiber neuron, which triggers last resort escapes immediately before an impending collision. One key property of these models is their prediction that peak neuronal responses occur at a fixed delay after the simulated approaching object reaches a threshold angular size on the retina. This prediction is valid for simulated objects approaching at a constant speed. We tested whether it remains valid when approaching objects accelerate. After characterizing and comparing the models’ responses to accelerating and constant speed stimuli, we find that the prediction holds true for the \(\kappa \) and the giant fiber model, but not for the \(\eta \) model. These results suggest that acceleration in the approach trajectory of an object may help distinguish and further constrain the neuronal computations required for collision avoidance in grasshoppers, fish and vinegar flies.

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Data availability

The MATLAB code required to reproduce all the figures and the statistical analysis of surrogate data for nonzero acceleration stimuli presented in Sec. 5 is available online at Mendeley Data (repository DOI: https://doi.org/10.17632/rvrz2tmf7j.1)).

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Acknowledgements

We would like to thank Dr. Gwyneth Card for sharing the data needed to compare NZAs with the acceleration values observed in damselflies during naturalistic prey capture experiments.

Funding

This study was supported by NSF Grant 2021795 and NIH Grant R01NS130917 to FG.

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Contributions

FG, TP and RD designed the work; FG carried out the mathematical derivations for model predictions and wrote the computer code to analyze the results; FG prepared the figures; and FG wrote the manuscript with input from TP and RD. All authors approved the final version of the manuscript. All persons designated as authors qualify for authorship, and all those who qualify for authorship are listed.

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Correspondence to Fabrizio Gabbiani.

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The authors have no conflicts of interest to report.

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Communicated by Benjamin Lindner.

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Gabbiani, F., Preuss, T. & Dewell, R.B. Approaching object acceleration differentially affects the predictions of neuronal collision avoidance models. Biol Cybern 117, 129–142 (2023). https://doi.org/10.1007/s00422-023-00961-0

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  • DOI: https://doi.org/10.1007/s00422-023-00961-0

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