Cited by 47Zebrafish Biomedical Research ApplicationsMemory and Neural MechanismsSpatial Cognition and Navigation

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Zebrafish Exploit Visual Cues and Geometric Relationships to Form a Spatial Memory

Open access

Published version of a preprint

Abstract

Animals use salient cues to navigate in their environment, but their specific cognitive strategies are largely unknown. We developed a conditioned place avoidance paradigm to discover whether and how zebrafish form spatial memories. In less than an hour, juvenile zebrafish, as young as 3 weeks, learned to avoid the arm of a Y-maze that was cued with a mild electric shock. Interestingly, individual fish solved this task in different ways: by staying in the safe center of the maze or by preference for one, or both, of the safe arms. In experiments in which the learned patterns were swapped, rotated, or replaced, the animals could transfer the association of safety to a different arm or to a different pattern using either visual cues or location as the conditioned stimulus. These findings show that juvenile zebrafish exhibit several complementary spatial learning modes, which generate a flexible repertoire of behavioral strategies.

Overview

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 · 10.1016/j.isci.2019.07.013

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Verification

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?

Self-check

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

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

Citations

Cites

Flagged first, then by citations

Show all 4 references

Research works printed but not linked: 37

  1. Aizenberg, 2011, Cerebellar-dependent learning in larval Zebrafish, J. Neurosci., 31, 8708, 10.1523/JNEUROSCI.6565-10.2011 · DOI
  2. Al-Imari, 2008, Sight of conspecifics as reward in associative learning in zebrafish (Danio rerio), Behav. Brain Res., 189, 216, 10.1016/j.bbr.2007.12.007 · DOI
  3. Aoki, 2015, Y-maze avoidance: an automated and rapid associative learning paradigm in zebrafish, Neurosci. Res., 91, 69, 10.1016/j.neures.2014.10.012 · DOI
  4. Bergmann, 2018, Imaging neuronal activity in the optic tectum of late stage larval Zebrafish, J. Dev. Biol., 6, 6, 10.3390/jdb6010006 · DOI
  5. Braubach, 2009, Olfactory conditioning in the zebrafish (Danio rerio), Behav. Brain Res., 198, 190, 10.1016/j.bbr.2008.10.044 · DOI
  6. Broglio, 2010, Selective involvement of the goldfish lateral pallium in spatial memory, Behav. Brain Res., 210, 191, 10.1016/j.bbr.2010.02.031 · DOI · Paper page
  7. Cheng, 1986, A purely geometric module in the rat’s spatial representation, Cognition, 23, 149, 10.1016/0010-0277(86)90041-7 · DOI
  8. Eichenbaum, 2017, The role of the hippocampus in navigation is memory, J. Neurophysiol., 117, 1785, 10.1152/jn.00005.2017 · DOI · Paper page
  9. Fanselow, 1990, Factors governing one-trial contextual conditioning, Anim. Learn. Behav., 18, 264, 10.3758/BF03205285 · DOI
  10. Franz, 2000, Biomimetic robot navigation, Rob. Auton. Syst., 30, 133, 10.1016/S0921-8890(99)00069-X · DOI · Paper page
  11. Gouteux, 2001, Rhesus monkeys use geometric and nongeometric information during a reorientation task, J. Exp. Psychol. Gen., 130, 505, 10.1037/0096-3445.130.3.505 · DOI
  12. Harmon, 2017, Distinct responses of Purkinje neurons and roles of simple spikes during associative motor learning in larval zebrafish, Elife, 6, 10.7554/eLife.22537 · DOI
  13. Hinz, 2013, Protein synthesis-dependent associative long-term memory in larval Zebrafish, J. Neurosci., 33, 15382, 10.1523/JNEUROSCI.0560-13.2013 · DOI
  14. Kalueff, 2013, Towards a comprehensive catalog of Zebrafish behavior 1.0 and beyond, Zebrafish, 10, 70, 10.1089/zeb.2012.0861 · DOI
  15. Kelly, 1998, Pigeons’ (Columba livia) encoding of geometric and featural properties of a spatial environment, J. Comp. Psychol., 112, 259, 10.1037/0735-7036.112.3.259 · DOI
  16. Kenney, 2017, Contextual fear conditioning in zebrafish, Learn. Mem., 24, 516, 10.1101/lm.045690.117 · DOI
  17. Lal, 2018, Identification of a neuronal population in the telencephalon essential for fear conditioning in zebrafish, BMC Biol., 16, 45, 10.1186/s12915-018-0502-y · DOI
  18. Lee, 2010, The Habenula prevents helpless behavior in larval Zebrafish, Curr. Biol., 20, 2211, 10.1016/j.cub.2010.11.025 · DOI
  19. Lee, 2012, Independent effects of geometry and landmark in a spontaneous reorientation task: a study of two species of fish, Anim. Cogn., 15, 861, 10.1007/s10071-012-0512-z · DOI
  20. Lee, 2013, Navigation by environmental geometry: the use of zebrafish as a model, J. Exp. Biol., 216, 3693
  21. Lee, 2015, Boundary primacy in spatial mapping: evidence from zebrafish (Danio rerio), Behav. Processes, 119, 116, 10.1016/j.beproc.2015.07.012 · DOI
  22. Liu, 2012, Alternative startle motor patterns and behaviors in the larval zebrafish (Danio rerio), J. Comp. Physiol. A, 198, 11, 10.1007/s00359-011-0682-1 · DOI
  23. López, 1999, Multiple spatial learning strategies in goldfish (Carassius auratus), Anim. Cogn., 2, 109, 10.1007/s100710050031 · DOI · Paper page
  24. Matsuda, 2017, Granule cells control recovery from classical conditioned fear responses in the zebrafish cerebellum, Sci. Rep., 7, 11865, 10.1038/s41598-017-10794-0 · DOI
  25. Mueller, 2011, The dorsal pallium in zebrafish, Danio rerio (Cyprinidae, Teleostei), Brain Res., 1381, 95, 10.1016/j.brainres.2010.12.089 · DOI
  26. O'Keefe, 1971, The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat, Brain Res., 34, 171, 10.1016/0006-8993(71)90358-1 · DOI · Paper page
  27. Packard, 1996, Inactivation of Hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning, Neurobiol. Learn. Mem., 65, 65, 10.1006/nlme.1996.0007 · DOI
  28. Poulos, 2009, Persistence of fear memory across time requires the basolateral amygdala complex, Proc. Natl. Acad. Sci. U S A, 106, 11737, 10.1073/pnas.0905257106 · DOI
  29. Salas, 2006, Neuropsychology of learning and memory in teleost fish, Zebrafish, 3, 157, 10.1089/zeb.2006.3.157 · DOI · Paper page
  30. Sison, 2010, Associative learning in zebrafish (Danio rerio) in the plus maze, Behav. Brain Res., 207, 99, 10.1016/j.bbr.2009.09.043 · DOI
  31. Tabor, 2014, Direct activation of the Mauthner cell by electric field pulses drives ultrarapid escape responses, J. Neurophysiol., 112, 834, 10.1152/jn.00228.2014 · DOI
  32. Temizer, 2015, A visual pathway for looming-evoked escape in larval Zebrafish, Curr. Biol., 25, 1823, 10.1016/j.cub.2015.06.002 · DOI · Paper page
  33. Valente, 2012, Ontogeny of classical and operant learning behaviors in zebrafish, Learn. Mem., 19, 170, 10.1101/lm.025668.112 · DOI
  34. Vallortigara, 1990, Geometric modules in animals’ spatial representations: a test with chicks (Gallus gallus domesticus), J. Comp. Psychol., 104, 248, 10.1037/0735-7036.104.3.248 · DOI
  35. Vargas, 2004, Encoding of geometric and featural spatial information by Goldfish (Carassius auratus), J. Comp. Psychol., 118, 206, 10.1037/0735-7036.118.2.206 · DOI · Paper page
  36. Vendrell-Llopis, 2016, Evolutionary conserved brainstem circuits encode category, concentration and mixtures of taste, Sci. Rep., 5, 17825, 10.1038/srep17825 · DOI
  37. Yang, 2019, Visual contrast modulates operant learning responses in larval Zebrafish, Front. Behav. Neurosci., 13, 4, 10.3389/fnbeh.2019.00004 · DOI

Cited by

Sorted by citations

See all 47

Metadata

Authors
Yashina, K., Tejero-Cantero, Á., Herz, A., & Baier, H.
Affiliations
  • Max Planck Institute of Neurobiology (DE)
  • Ludwig-Maximilians-Universität München (DE)
Corresponding author
Baier, Herwig
Venue
iScience
Publisher
Elsevier BV
Published
2019-09
Volume
19
Pages
119-134
ISSN
2589-0042 (ISSN-L)
OpenAlex
W2958418972
Cited by
47
References
4
Citations by year
2026: 6 · 2025: 8 · 2024: 5 · 2023: 8 · 2022: 5 · 2021: 8 · 2020: 7
FWCI
2.65
Type
journal article
Language
en
Open access
Locations
  • iScience (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders
  • Max-Planck-Gesellschaft
  • Deutsche Forschungsgemeinschaft (RTG 2175)
  • Bundesministerium für Bildung und Forschung
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Spatial Cognition and Navigation
Keywords
zebrafish, spatial memory, spatial learning, conditioned place avoidance, visual cues, geometric cues, Y-maze, juvenile fish, transfer of learning, behavioral strategies

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