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      Dual Receptive Fields Underlying Target and Wide-Field Motion Sensitivity in Looming-Sensitive Descending Neurons

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          Abstract

          Responding rapidly to visual stimuli is fundamental for many animals. For example, predatory birds and insects alike have amazing target detection abilities, with incredibly short neural and behavioral delays, enabling efficient prey capture. Similarly, looming objects need to be rapidly avoided to ensure immediate survival, as these could represent approaching predators. Male Eristalis tenax hoverflies are nonpredatory, highly territorial insects that perform high-speed pursuits of conspecifics and other territorial intruders. During the initial stages of the pursuit, the retinal projection of the target is very small, but this grows to a larger object before physical interaction. Supporting such behaviors, E. tenax and other insects have both target-tuned and loom-sensitive neurons in the optic lobes and the descending pathways. We here show that these visual stimuli are not necessarily encoded in parallel. Indeed, we describe a class of descending neurons that respond to small targets, to looming and to wide-field stimuli. We show that these descending neurons have two distinct receptive fields where the dorsal receptive field is sensitive to the motion of small targets and the ventral receptive field responds to larger objects or wide-field stimuli. Our data suggest that the two receptive fields have different presynaptic input, where the inputs are not linearly summed. This novel and unique arrangement could support different behaviors, including obstacle avoidance, flower landing, and target pursuit or capture.

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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                10 July 2023
                21 July 2023
                July 2023
                : 10
                : 7
                : ENEURO.0188-23.2023
                Affiliations
                [1 ]Flinders Health and Medical Research Institute, Flinders University , Adelaide 5001, Australia
                [2 ]Department of Medical Cell Biology, Uppsala University , 75123 Uppsala, Sweden
                Author notes

                The authors declare no competing financial interests.

                Author contributions: S.N. and K.N. designed research; S.N. and Y.O. performed research; K.N. contributed unpublished reagents/analytic tools; S.N. analyzed data; S.N., Y.O., and K.N. wrote the paper.

                This research was funded by the US Air Force Office of Scientific Research (Grant FA9550-19-1-0294) and the Australian Research Council (Grants DP180100144, DP210100740, DP230100006, and FT180100289).

                Correspondence should be addressed to Karin Nordström at karin.nordstrom@ 123456flinders.edu.au .
                Article
                eN-NWR-0188-23
                10.1523/ENEURO.0188-23.2023
                10368147
                37429705
                455ae63e-ae88-4b19-8e4c-8ee160991f35
                Copyright © 2023 Nicholas et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 31 May 2023
                : 16 June 2023
                Page count
                Figures: 12, Tables: 0, Equations: 0, References: 56, Pages: 15, Words: 00
                Funding
                Funded by: DOD | USAF | AMC | Air Force Office of Scientific Research (AFOSR), doi 10.13039/100000181;
                Award ID: FA9550-19-1-0294
                Funded by: Australian Research Council
                Award ID: DP180100144
                Award ID: DP210100740
                Award ID: DP230100006 and FT1801002
                Categories
                8
                Research Article: New Research
                Sensory and Motor Systems
                Custom metadata
                July 2023

                descending neuron,hoverfly,insect vision,motion vision,target motion,wide-field motion

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