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Flight-induced compass representation in the monarch butterfly heading network

Beetz, M. Jerome ; Kraus, Christian ; Franzke, Myriam ; Dreyer, David LU ; Strube-Bloss, Martin F. ; Rössler, Wolfgang ; Warrant, Eric J. LU orcid ; Merlin, Christine and el Jundi, Basil LU (2022) In Current Biology 32(2). p.5-349
Abstract

For navigation, animals use a robust internal compass. Compass navigation is crucial for long-distance migrating animals like monarch butterflies, which use the sun to navigate over 4,000 km to their overwintering sites every fall. Sun-compass neurons of the central complex have only been recorded in immobile butterflies, and experimental evidence for encoding the animal's heading in these neurons is still missing. Although the activity of central-complex neurons exhibits a locomotor-dependent modulation in many insects, the function of such modulations remains unexplored. Here, we developed tetrode recordings from tethered flying monarch butterflies to reveal how flight modulates heading representation. We found that, during flight,... (More)

For navigation, animals use a robust internal compass. Compass navigation is crucial for long-distance migrating animals like monarch butterflies, which use the sun to navigate over 4,000 km to their overwintering sites every fall. Sun-compass neurons of the central complex have only been recorded in immobile butterflies, and experimental evidence for encoding the animal's heading in these neurons is still missing. Although the activity of central-complex neurons exhibits a locomotor-dependent modulation in many insects, the function of such modulations remains unexplored. Here, we developed tetrode recordings from tethered flying monarch butterflies to reveal how flight modulates heading representation. We found that, during flight, heading-direction neurons change their tuning, transforming the central-complex network to function as a global compass. This compass is characterized by the dominance of processing steering feedback and allows for robust heading representation even under unreliable visual scenarios, an ideal strategy for maintaining a migratory heading over enormous distances.

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author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
central complex, heading coding, migration, navigation, octopamine, orientation, state-dependence, sun compass, tetrode recordings
in
Current Biology
volume
32
issue
2
pages
5 - 349
publisher
Elsevier
external identifiers
  • pmid:34822766
  • scopus:85123180274
ISSN
0960-9822
DOI
10.1016/j.cub.2021.11.009
language
English
LU publication?
yes
id
15c1b50d-96e5-41e7-a5ca-3d74af4cc994
date added to LUP
2022-05-12 12:38:20
date last changed
2024-04-18 07:21:58
@article{15c1b50d-96e5-41e7-a5ca-3d74af4cc994,
  abstract     = {{<p>For navigation, animals use a robust internal compass. Compass navigation is crucial for long-distance migrating animals like monarch butterflies, which use the sun to navigate over 4,000 km to their overwintering sites every fall. Sun-compass neurons of the central complex have only been recorded in immobile butterflies, and experimental evidence for encoding the animal's heading in these neurons is still missing. Although the activity of central-complex neurons exhibits a locomotor-dependent modulation in many insects, the function of such modulations remains unexplored. Here, we developed tetrode recordings from tethered flying monarch butterflies to reveal how flight modulates heading representation. We found that, during flight, heading-direction neurons change their tuning, transforming the central-complex network to function as a global compass. This compass is characterized by the dominance of processing steering feedback and allows for robust heading representation even under unreliable visual scenarios, an ideal strategy for maintaining a migratory heading over enormous distances.</p>}},
  author       = {{Beetz, M. Jerome and Kraus, Christian and Franzke, Myriam and Dreyer, David and Strube-Bloss, Martin F. and Rössler, Wolfgang and Warrant, Eric J. and Merlin, Christine and el Jundi, Basil}},
  issn         = {{0960-9822}},
  keywords     = {{central complex; heading coding; migration; navigation; octopamine; orientation; state-dependence; sun compass; tetrode recordings}},
  language     = {{eng}},
  month        = {{01}},
  number       = {{2}},
  pages        = {{5--349}},
  publisher    = {{Elsevier}},
  series       = {{Current Biology}},
  title        = {{Flight-induced compass representation in the monarch butterfly heading network}},
  url          = {{http://dx.doi.org/10.1016/j.cub.2021.11.009}},
  doi          = {{10.1016/j.cub.2021.11.009}},
  volume       = {{32}},
  year         = {{2022}},
}