Binocular Encoding in the Damselfly Pre-motor Target Tracking System

Jack A. Supple, Daniel Pinto-Benito, Christopher Khoo, Trevor J. Wardill, Samuel T. Fabian, Molly Liu, Siddhant Pusdekar, Daniel Galeano, Jintao Pan, Shengdian Jiang, Yimin Wang, Lijuan Liu, Hanchuan Peng, Robert M. Olberg, Paloma T. Gonzalez-Bellido

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Akin to all damselflies, Calopteryx (family Calopterygidae), commonly known as jewel wings or demoiselles, possess dichoptic (separated) eyes with overlapping visual fields of view. In contrast, many dragonfly species possess holoptic (dorsally fused) eyes with limited binocular overlap. We have here compared the neuronal correlates of target tracking between damselfly and dragonfly sister lineages and linked these changes in visual overlap to pre-motor neural adaptations. Although dragonflies attack prey dorsally, we show that demoiselles attack prey frontally. We identify demoiselle target-selective descending neurons (TSDNs) with matching frontal visual receptive fields, anatomically and functionally homologous to the dorsally positioned dragonfly TSDNs. By manipulating visual input using eyepatches and prisms, we show that moving target information at the pre-motor level depends on binocular summation in demoiselles. Consequently, demoiselles encode directional information in a binocularly fused frame of reference such that information of a target moving toward the midline in the left eye is fused with information of the target moving away from the midline in the right eye. This contrasts with dragonfly TSDNs, where receptive fields possess a sharp midline boundary, confining responses to a single visual hemifield in a sagittal frame of reference (i.e., relative to the midline). Our results indicate that, although TSDNs are conserved across Odonata, their neural inputs, and thus the upstream organization of the target tracking system, differ significantly and match divergence in eye design and predatory strategies. Video Abstract:[Figure presented] Supple et al. link the divergent eye morphology and hunting strategies of dragonflies and damselflies. Target-selective descending neurons in these two groups are identified as homologous, but damselfly TSDNs face forward and encode information in a binocular-fused reference frame.

Original languageEnglish (US)
Pages (from-to)645-656.e4
JournalCurrent Biology
Volume30
Issue number4
DOIs
StatePublished - Feb 24 2020

Bibliographical note

Funding Information:
This work was funded by the Air Force Office of Scientific Research (FA9550-15-1-0188 to P.T.G.B. and Karin Nordstr?m and FA9550-18-1-0339 to P.T.G.B. and T.J.W.) and the Biotechnology and Biological Sciences Research Council (grant numbers BB/M011194/1 to J.A.S. and BB/L024667/1 to T.J.W.). This work was also supported by funding from the University of Minnesota College of Biological Sciences to P.T.G.B. and T.J.W. We thank Andrea Worthington for crucial support during the intracellular recording experiments, Francis Velasquez for his continuous logistic support, staff at Nixon Park for supporting fieldwork, York College for kindly providing us access to their facilities, and the University of Minnesota insect collection for kindly allowing access to Odonata specimens. Special thanks to Mary Sumner for help with rearing damselflies and dragonflies in the lab and to Abril K. Bellido-Wardill for her help during the dragonfly behavioral experiments. J.A.S. C.K. T.J.W. and P.T.G.-B. designed the study. J.A.S. S.T.F. M.L. D.G. and S.P. collected behavioral data. J.A.S. and S.P. analyzed the behavioral data. J.A.S. and D.P.-B. carried out the extracellular experiments and analyzed the data. P.T.G.-B. and R.M.O. carried out the intracellular recordings, and R.M.O. and J.A.S. analyzed the data. J.A.S. T.J.W. and P.T.G.-B. processed and imaged the brain samples. H.P. and Y.W. developed tools for neuron reconstruction and profiling. H.P. and L.L. managed the generation of reconstructions of J.P. and S.J. and performed the proofreading. J.A.S. and P.T.G.-B. wrote the first draft. The authors declare no competing interests.

Funding Information:
This work was funded by the Air Force Office of Scientific Research ( FA9550-15-1-0188 to P.T.G.B. and Karin Nordström and FA9550-18-1-0339 to P.T.G.B. and T.J.W.) and the Biotechnology and Biological Sciences Research Council (grant numbers BB/M011194/1 to J.A.S. and BB/L024667/1 to T.J.W.). This work was also supported by funding from the University of Minnesota College of Biological Sciences to P.T.G.B. and T.J.W. We thank Andrea Worthington for crucial support during the intracellular recording experiments, Francis Velasquez for his continuous logistic support, staff at Nixon Park for supporting fieldwork, York College for kindly providing us access to their facilities, and the University of Minnesota insect collection for kindly allowing access to Odonata specimens. Special thanks to Mary Sumner for help with rearing damselflies and dragonflies in the lab and to Abril K. Bellido-Wardill for her help during the dragonfly behavioral experiments.

Keywords

  • TSDN
  • demoiselle
  • evolution
  • flight
  • invertebrate
  • jewel wing
  • predation
  • reference frame
  • summation
  • vision

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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