Cited by 162Spatial Cognition and NavigationNeurobiology and Insect Physiology ResearchMemory and Neural Mechanisms

No Need for a Cognitive Map: Decentralized Memory for Insect Navigation

Open access
Cruse, Holk, Wehner, Rüdiger·2011·PLoS Computational Biology

Abstract

In many animals the ability to navigate over long distances is an important prerequisite for foraging. For example, it is widely accepted that desert ants and honey bees, but also mammals, use path integration for finding the way back to their home site. It is however a matter of a long standing debate whether animals in addition are able to acquire and use so called cognitive maps. Such a 'map', a global spatial representation of the foraging area, is generally assumed to allow the animal to find shortcuts between two sites although the direct connection has never been travelled before. Using the artificial neural network approach, here we develop an artificial memory system which is based on path integration and various landmark guidance mechanisms (a bank of individual and independent landmark-defined memory elements). Activation of the individual memory elements depends on a separate motivation network and an, in part, asymmetrical lateral inhibition network. The information concerning the absolute position of the agent is present, but resides in a separate memory that can only be used by the path integration subsystem to control the behaviour, but cannot be used for computational purposes with other memory elements of the system. Thus, in this simulation there is no neural basis of a cognitive map. Nevertheless, an agent controlled by this network is able to accomplish various navigational tasks known from ants and bees and often discussed as being dependent on a cognitive map. For example, map-like behaviour as observed in honey bees arises as an emergent property from a decentralized system. This behaviour thus can be explained without referring to the assumption that a cognitive map, a coherent representation of foraging space, must exist. We hypothesize that the proposed network essentially resides in the mushroom bodies of the insect brain.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pcbi.1002009

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Ants forage for food along meandering paths but take near-optimal return trips, though there is controversy about whether insects like ants and bees are capable of forming maps.

    “Ants forage for food along meandering paths but take near-optimal return trips (Müller & Wehner, 1988), though there is some controversy about whether insects like ants and bees are capable of forming maps (Cruse & Wehner, 2011; Cheung et al., 2014).”

    From Emergence of Maps in the Memories of Blind Navigation Agents (2023) · cites this paper as Cruse & Wehner, 2011

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 43

  1. [1]Wehner R 2003 Desert ant navigation: how miniature brains solve complex tasks. Karl von Frisch Lecture. J Comp Physiol A 189 579 588 12879352
  2. [4]Cheng K Narendra A Sommer S Wehner R 2009 Traveling in clutter: navigation in the central Australian desert ant Melophorus bagoti. Behav Processes 80 261 268 19049857
  3. [5]Wehner R Labhart T 2006 Polarization vision. Warrant E Nilsson D-E Invertebrate Vision Cambridge UK Cambridge University Press 291 348
  4. [7]Wittlinger M Wehner R Wolf H 2007 The ant odometer: stepping on stilts and stumps. Science 312 1965 1967 16809544
  5. [8]Wehner R Srinivasan MV 2003 Path integration in insects. Jeffery KJ The Neurobiology of Spatial Behaviour Oxford Oxford University Press 9 30
  6. [9]Sommer S Wehner R 2004 The ant's estimation of distance travelled: experiments with desert ants, Cataglyphis fortis. J Comp Physiol A 190 1 6 14614570
  7. [10]Wehner R Michel B Antonsen P 1996 Visual navigation in insects: coupling egocentric and geocentric information. J Exp Biol 199 129 140 9317483
  8. [11]Sommer S Beeren C von Wehner R 2008 Multiroute memories in desert ants. Proc Natl Acad Sci USA 105 317 322 18160534 PMC2224209
  9. [14]Merkle T Knaden M Wehner R 2006 Uncertainty about nest position influences systematic search in desert ants. J Exp Biol 209 3545 3549 16943494
  10. [17]Gould JL 1986 The locale map of honey bees: do insects have cognitive maps? Science 232 861 863 17755968
  11. [18]Menzel R Brandt R Gumbert A Komischke B Kunze J 2000 The spatial memories for honeybee navigation. Proc R Soc Lond B 267 961 968 PMC1690634 10874744
  12. [19]Menzel R Greggers U Smith A Berger S Brandt R 2005 Honey bees navigate according to a map-like spatial memory. Proc Natl Acad Sci USA 102 3040 3045 15710880 PMC549458
  13. [21]Wehner R Boyer M Loertscher F Sommer S Menzi U 2006 Desert ant navigation: one-way routes rather than maps. Curr Biol 16 75 79 16401425
  14. [22]Menzel R Giurfa M 2001 Cognitive architecture of a mini-brain: the honeybee. Trends Cogn Sci 5 62 71 11166636
  15. [24]Cleeremans A 2005 Computational correlates of consciousness. Prog Brain Res 150 81 98 16186017
  16. [25]Cruse H Schilling M 2010 Getting cognitive. Bläsing B Puttke M Schack T The Neurocognition of Dance London Psychology Press 53 74
  17. [26]Wehner R 1983 Celestial and terrestrial navigation: human strategies – insect strategies. Huber F Markl H Neuroethology and Behavioral Physiology Heidelberg, New York Springer 366 381
  18. [27]Collett M Collett TS 2000 How do insects use path integration for their navigation? Biol Cybern 83 245 259 11007299
  19. [30]Vickerstaff R J Cheung A 2010 Which coordinate system for modelling path integration? J Theor Biol 263 242 261 19962387
  20. [31]Kohler M Wehner R 2005 Idiosyncratic route-based memories in desert ants, Melophorus bagoti: how do they interact with path-integration vectors? Neurobiol Learn Mem 83 1 12 15607683
  21. [32]Bisch-Knaden S Wehner R 2003 Local vectors in desert ants: context dependent landmark learning during outbound and homebound runs. J Comp Physiol A 189 181 187 12664094
  22. [33]Collett M Collett TS 2010 The learning and maintenance of local vectors in desert ant navigation. J Exp Biol 212 895 900 19282485
  23. [34]Cruse H Hübner D 2008 Selforganizing memory: active learning of landmarks used for navigation. Biol Cybern 99 219 236 18797951
  24. [35]Kühn S Beyn W-J Cruse H 2007 Modelling Memory Functions with recurrent neural networks consisting of input compensation units. I. Static situations. Biol Cybern 96 455 470 17211628
  25. [36]Makarov VA Song Y Velarde MG Hübner D Cruse H 2008 Elements for a general memory structure: Properties of recurrent neural networks used to form situation models. Biol Cybern 98 371 395 18350312
  26. [38]Möller R Vardy A 2006 Local visual homing by matched-filter descent in image distances. Biol Cybern 95 413 430 17021827
  27. [39]Basten K Mallot HA 2010 Simulated visual homing in desert ant natural environments: efficiency of skyline cues. Biol Cybern 102 413 425 20300942
  28. [40]Cheung A Vickerstaff R 2010 Finding the Way with a Noisy Brain. PLoS Comput Biol 6 e1000992 21085678 PMC2978673
  29. [42]Cruse H 2002 The functional sense of “central oscillations” in walking. Biol Cybern 86 271 280 11956808
  30. [43]Dürr V Schmitz J Cruse H 2004 Behaviour-based modelling of hexapod locomotion: Linking biology and technical application. Arthropod Struct Develop 33 237 250 18089037
  31. [44]Menzel R Brembs B Giufra M 2007 Cognition in invertebrates. Kaas JH Evolution of nervous systems 403 442 Volume 2: Evolution of nervous systems in invertebrates. Academic press, New York
  32. [45]Strausfeld NJ Sinakevitch I Brown SM Farris SM 2009 Ground plan of the insect mushroom body: functional and evolutionary implications. J Comp Neurol 513 265 291 19152379 PMC4876875
  33. [46]Strausfeld NJ 2001 Insect brains. Roth G Wullimann MF Brain Evol Cogn New York Wiley 367 420
  34. [47]Heisenberg M 2003 Mushroom body memoir: from maps to models. Nature Rev Neurosc 4 266 275 12671643
  35. [48]Krofczik S Khojasteh U Hempel de Ibarra N Menzel R 2008 Adaptation of microglomerular complexes in the honeybee mushroom body lip to manipulations of behavioural maturation and sensory experience. Dev Neurobiol 68 1007 1017 18446779
  36. [50]Seid MA Wehner R 2009 Delayed axonal pruning in the ant brain: a study of developmental trajectories. Dev Neurobiol 69 1 15 19263416
  37. [51]Stieb SM Münz TS Wehner R Rössler W 2010 Visual experience and age affect synaptic organization in the mushroom bodies of the desert ant Cataglyphis fortis. Dev Neurobiol 70 408 423 20131320
  38. [52]Strausfeld NJ Hansen L Li Y Gomez RS Ito K 1998 Evolution, discovery, and interpretation of arthropod mushroom bodies. Learn Mem 5 11 37 10454370 PMC311242
  39. [53]Liu L Wolf R Ernst R Heisenberg M 1999 Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400 753 756 10466722
  40. [54]Tang S Guo A 2001 Choice behavior of Drosophila facing contradictory visual cues. Science 294 1543 1547 11711680
  41. [55]Strausfeld NJ 1999 A brain region in the insect that supervises walking. Progr Brain Res 123 273 284 10635723
  42. [56]Strauss R 2002 The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12 633 638 12490252
  43. [57]Homberg U 2008 Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37 347 362 18502176

Cited by

Sorted by citations

Authors
Cruse, H., & Wehner, R.
Affiliations
  • Bielefeld University (DE)
  • University of Zurich (CH)
Corresponding author
Cruse, Holk
Venue
PLoS Computational Biology
Published
2011-03-17
Volume
7
Issue
3
Pages
e1002009
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
OpenAlex
W2118686323
Cited by
162
References
2
Citations by year
2026: 6 · 2025: 4 · 2024: 10 · 2023: 10 · 2022: 5 · 2021: 9 · 2020: 12 · 2019: 15 · 2018: 12 · 2017: 10 · 2016: 6 · 2015: 8 · 2014: 16 · 2013: 17 · 2012: 18
FWCI
35.99
Type
journal article
Language
en
Open access
Locations
  • PLoS Computational Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by)
  • PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion)
Funders
Alexander von Humboldt-Stiftung
Topics
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
insect navigation, cognitive maps, path integration, artificial neural network model, lateral inhibition, desert ants, Apis mellifera, mushroom body, emergent behavior, foraging
MeSH terms
Animals, Ants, Appetitive Behavior, Bees, Homing Behavior, Memory, Models, Biological, Space Perception, Computational Biology

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review