Non-linear neuronal responses as an emergent property of afferent networks:a case study of the locust lobula giant movement detector

Abstract

In principle it appears advantageous for single neurons to perform non-linear operations. Indeed it has been reported that some neurons show signatures of such operations in their electrophysiological response. A particular case in point is the Lobula Giant Movement Detector (LGMD) neuron of the locust, which is reported to locally perform a functional multiplication. Given the wide ramifications of this suggestion with respect to our understanding of neuronal computations, it is essential that this interpretation of the LGMD as a local multiplication unit is thoroughly tested. Here we evaluate an alternative model that tests the hypothesis that the non-linear responses of the LGMD neuron emerge from the interactions of many neurons in the opto-motor processing structure of the locust. We show, by exposing our model to standard LGMD stimulation protocols, that the properties of the LGMD that were seen as a hallmark of local non-linear operations can be explained as emerging from the dynamics of the pre-synaptic network. Moreover, we demonstrate that these properties strongly depend on the details of the synaptic projections from the medulla to the LGMD. From these observations we deduce a number of testable predictions. To assess the real-time properties of our model we applied it to a high-speed robot. These robot results show that our model of the locust opto-motor system is able to reliably stabilize the movement trajectory of the robot and can robustly support collision avoidance. In addition, these behavioural experiments suggest that the emergent non-linear responses of the LGMD neuron enhance the system's collision detection acuity. We show how all reported properties of this neuron are consistently reproduced by this alternative model, and how they emerge from the overall opto-motor processing structure of the locust. Hence, our results propose an alternative view on neuronal computation that emphasizes the network properties as opposed to the local transformations that can be performed by single neurons.

Publication DOI: https://doi.org/10.1371/journal.pcbi.1000701
Divisions: College of Engineering & Physical Sciences
Additional Information: © 2010 Bermu´dez i Badia et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Uncontrolled Keywords: Action Potentials,Animals,Computer Simulation,Grasshoppers,Models, Neurological,Motion Perception,Nerve Net,Neurons, Afferent,Nonlinear Dynamics,Sense Organs,Journal Article,Research Support, Non-U.S. Gov't
Publication ISSN: 1553-7358
Last Modified: 03 Dec 2024 08:12
Date Deposited: 06 Apr 2018 12:40
Full Text Link:
Related URLs: http://journals ... al.pcbi.1000701 (Publisher URL)
PURE Output Type: Article
Published Date: 2010-03-12
Authors: Bermúdez i Badia, Sergi
Bernardet, Ulysses (ORCID Profile 0000-0003-4659-3035)
Verschure, Paul F M J

Download

[img]

Version: Published Version

License: Creative Commons Attribution

| Preview

Export / Share Citation


Statistics

Additional statistics for this record