Cited by 165Neurobiology and Insect Physiology ResearchVisual perception and processing mechanismsMemory and Neural Mechanisms

Sensorimotor experience remaps visual input to a heading-direction network

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Fisher, Yvette E., Lu, Jenny, D’Alessandro, Isabel, Wilson, Rachel I.·2019·Nature

Abstract

In the Drosophila brain, 'compass' neurons track the orientation of the body and head (the fly's heading) during navigation 1,2. In the absence of visual cues, the compass neuron network estimates heading by integrating self-movement signals over time 3,4. When a visual cue is present, the estimate of the network is more accurate 1,3. Visual inputs to compass neurons are thought to originate from inhibitory neurons called R neurons (also known as ring neurons); the receptive fields of R neurons tile visual space 5. The axon of each R neuron overlaps with the dendrites of every compass neuron 6, raising the question of how visual cues are integrated into the compass. Here, using in vivo whole-cell recordings, we show that a visual cue can evoke synaptic inhibition in compass neurons and that R neurons mediate this inhibition. Each compass neuron is inhibited only by specific visual cue positions, indicating that many potential connections from R neurons onto compass neurons are actually weak or silent. We also show that the pattern of visually evoked inhibition can reorganize over minutes as the fly explores an altered virtual-reality environment. Using ensemble calcium imaging, we demonstrate that this reorganization causes persistent changes in the compass coordinate frame. Taken together, our data suggest a model in which correlated pre- and postsynaptic activity triggers associative long-term synaptic depression of visually evoked inhibition in compass neurons. Our findings provide evidence for the theoretical proposal that associative plasticity of sensory inputs, when combined with attractor dynamics, can reconcile self-movement information with changing external cues to generate a coherent sense of direction 7-12.

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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].”

    From A model of cue integration as vector summation in the insect brain (2023) · cites this paper as [16]

    The Results (page not provided) show that experience changes E-PG visual receptive fields, supporting flexible remapping. They identify R→E-PG synapses as the most likely site of plasticity, while the Discussion proposes a synaptic learning mechanism; the paper does not establish plasticity at those specific connections as a demonstrated fact. The all-to-all anatomical arrangement is described in the Abstract, though separate citations accompany that clause in the citing sentence. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • Hebbian learning is often suggested for the construction of R→E-PG mappings.

    “Hebbian learning is often suggested for the construction of R → E-PG mappings [16,17,19,20,28,41]).”
  • 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].”
  • No statistical methods were used to predetermine sample sizes, but the sample sizes are similar to those reported in previous publications.

    “No statistical methods were used to predetermine sample sizes but our sample sizes are similar to those reported in previous publications23,24,33,34,37,38.”

    From Multimodal cue integration and learning in a neural representation of head direction (2025) · cites this paper as [23]

    Experimental — accuracy not yet measured
  • 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.”

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Authors
Fisher, Y. E., Lu, J., D’Alessandro, I., & Wilson, R. I.
Affiliations
Harvard University (US)
Corresponding author
Wilson, Rachel I.
Venue
Nature
Published
2019-11-20
Volume
576
Issue
7785
Pages
121-125
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2990686989
Cited by
165
References
56
Citations by year
2026: 17 · 2025: 18 · 2024: 23 · 2023: 23 · 2022: 27 · 2021: 26 · 2020: 25 · 2019: 6
FWCI
9.98
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Digital Access to Scholarship at Harvard (DASH) (Harvard University) (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • National Eye Institute (P30EY012196)
  • National Institute on Deafness and Other Communication Disorders (F30DC017698)
  • National Institute of General Medical Sciences (T32GM007753)
  • National Institute of Neurological Disorders and Stroke (P30NS072030, U19NS104655)
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
heading direction, visual cue integration, synaptic inhibition, associative plasticity, long-term depression, attractor dynamics, sensorimotor integration, whole-cell recording, calcium imaging
MeSH terms
Animals, Drosophila melanogaster, Head, Motor Activity, Movement, Neurons, Vision, Ocular

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