Cited by 172Neurobiology and Insect Physiology ResearchVisual perception and processing mechanismsMemory and Neural Mechanisms

Generation of stable heading representations in diverse visual scenes

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Kim, Sung Soo, Hermundstad, Ann M., Romani, Sandro, Abbott, L. F., Jayaraman, Vivek·2019·Nature

Abstract

Many animals rely on an internal heading representation when navigating in varied environments 1-10. How this representation is linked to the sensory cues that define different surroundings is unclear. In the fly brain, heading is represented by 'compass' neurons that innervate a ring-shaped structure known as the ellipsoid body 3,11,12. Each compass neuron receives inputs from 'ring' neurons that are selective for particular visual features 13-16; this combination provides an ideal substrate for the extraction of directional information from a visual scene. Here we combine two-photon calcium imaging and optogenetics in tethered flying flies with circuit modelling, and show how the correlated activity of compass and visual neurons drives plasticity 17-22, which flexibly transforms two-dimensional visual cues into a stable heading representation. We also describe how this plasticity enables the fly to convert a partial heading representation, established from orienting within part of a novel setting, into a complete heading representation. Our results provide mechanistic insight into the memory-related computations that are essential for flexible navigation in varied surroundings.

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  • Each R neuron connects to all E-PGs and these connections are plastic, enabling flexible remapping of the outside world onto the compass neurons.

    “Each R neuron connects to all E-PGs [13,19] and these connections are plastic, enabling flexible remapping of the outside world onto the compass neurons [16,20,21].”
  • The lack of plasticity in [43] does not reflect known phenomena in fruit flies and dung beetles.

    “This is noted as a strength of the model (conceptual simplicity), however, it does not reflect known phenomena in fruit flies and dung beetles [16,20,22].”
  • As cues change and learning proceeds, changes in synaptic weights and resulting changes in profile are expected.

    “Thus, as cues change and learning proceeds, we might expect to see changes in synaptic weights20–28 and resulting changes in profile49,50.”
  • Most previous models do not investigate multi-cue behaviour.

    “Most previous models do not investigate multi-cue behaviour [8,20,28,42].”

    From A model of cue integration as vector summation in the insect brain (2023) · cites this paper as [20]

    The ‘Attractor model with plasticity creates a stable visual-motor compass’ section describes this paper’s model and mentions earlier models, but does not assess whether most previous models investigate multi-cue behaviour. The ‘Stability of heading representation in 2D visual scenes’ section discusses multiple visual maps and other possible sensory cues, not the prevalence of multi-cue work in previous models. No page numbers are available in our copy. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 2

  1. [29]Green J, Vijayan V, Mussells Pires P, Adachi A. & Maimon G. A neural heading estimate is compared with an internal goal to guide oriented navigation. Nat Neurosci 22, 1460– 1468 (2019). 31332373 PMC7688015
  2. [39]Buchner E. Dunkelanregung des stationaeren flugs der fruchtfliege Drosophila. Dipl. thesis. Univ Tübingen (1971).

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Authors
Kim, S. S., Hermundstad, A. M., Romani, S., Abbott, L. F., & Jayaraman, V.
Affiliations
Howard Hughes Medical Institute (US)
Corresponding author
  • Kim, Sung Soo
  • Jayaraman, Vivek
Venue
Nature
Published
2019-11-20
Volume
576
Issue
7785
Pages
126-131
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2991430622
Cited by
172
References
61
Citations by year
2026: 29 · 2025: 17 · 2024: 32 · 2023: 21 · 2022: 22 · 2021: 21 · 2020: 24 · 2019: 6
FWCI
8.72
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health (2t32ns064929-16a1)
  • National Institute of Neurological Disorders and Stroke (T32-NS-064929)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
ellipsoid body, visual navigation, neuroplasticity, Drosophila, circuit modeling, optogenetics, tethered flight
MeSH terms
Orientation, Spatial, Animals, Calcium, Drosophila melanogaster, Head, Neuronal Plasticity, Neurons, Visual Perception, Optogenetics

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