CoChat
Sign Up
Cited by 163Memory and Neural MechanismsSpatial Cognition and NavigationNeurogenesis and neuroplasticity mechanisms

Neural representations of space in the hippocampus of a food-caching bird

Open access
Payne, H. L., Lynch, G. F., Aronov, D.·2021·Science
DOI 10.1126/science.abg2009PMC PMC8503942

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Conserved spatial memory mechanisms: Food-caching birds are memory specialists that can remember thousands of hidden food items. Using electrophysiological recordings from freely behaving birds, Payne et al. analyzed neuronal activity in the likely hippocampus homolog of two bird species, the tufted titmouse and the zebra finch. They chose these two species to compare, respectively, birds that do and do not display food-caching behavior. Place cells and typical hippocampal firing patterns that resembled rodent neuronal activity could be detected in the extreme memory specialists. Compared with titmice, however, spatial activity was noticeably weaker and less abundant in zebra finches. These findings provide evidence that the neural processes underlying spatial memory are remarkably conserved across widely divergent hippocampal circuits separated by millions of years of evolution. Science , abg2009, this issue p. 343

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 · 10.1126/science.abg2009

Cites

9 of 9 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?

  • The criteria used for PC identification are similar to those in the existing literature in both mammals and birds, for both electrophysiological and calcium imaging data.

    “The criteria we use are similar to those in the existing literature in both mammals and birds, for both electrophysiological and calcium imaging data16,53.”

    From A population code for spatial representation in the zebrafish telencephalon (2024) · cites this paper as [16]

    The passage labeled Abstract (page unavailable) says the bird electrophysiology study used conventional spatial-information and spatial-stability criteria to identify place cells, supporting that part of the comparison with existing literature. It does not address whether those criteria are similar to ones used with calcium-imaging data. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • The previous lack of evidence for PCs outside mammalian and avian species suggests either that the neural architecture needed to generate PCs evolved following the emergence of land vertebrates or that PCs in species such as teleost fish have not yet been discovered due to methodological limitations.

    “The previous lack of evidence for PCs outside of mammalian and avian species suggests either that the neural architecture needed to generate PCs evolved following the emergence of land vertebrates5,16 or that PCs in species such as teleost fish have not yet been discovered, potentially due to methodological limitations (for example, sparse recordings or tethered preparations).”

    From A population code for spatial representation in the zebrafish telencephalon (2024) · cites this paper as [16]

    The paper’s discussion of earlier non-mammalian recordings (section labeled Abstract; page unavailable) says classic place cells had not been reported and considers both fundamentally different mechanisms and place cells that are difficult to detect. It does not date the evolution of place-cell circuitry to the emergence of land vertebrates or identify sparse recordings or tethered preparations as reasons place cells have not been found in teleost fish; its sparse-sampling example concerns birds. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • PCs have been comprehensively identified only in the hippocampus of birds and mammals.

    “Notably, PCs have been comprehensively identified only in the hippocampus of birds16 and mammals5,17.”

    From A population code for spatial representation in the zebrafish telencephalon (2024) · cites this paper as [16]

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: 39

  1. [1]Morris RGM, Garrud P, Rawlins JNP, O’Keefe J, Place navigation impaired in rats with hippocampal lesions. Nature. 297, 681– 683 (1982). 7088155
  2. [4]Rodríguez F, López JC, Vargas JP, Broglio C, Gómez Y, Salas C, Spatial memory and hippocampal pallium through vertebrate evolution: Insights from reptiles and teleost fish. Brain Res. Bull 57, 499– 503 (2002). 11923018
  3. [5]Tosches MA, Yamawaki TM, Naumann RK, Jacobi AA, Tushev G, Laurent G, Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science. 360, 881– 888 (2018). 29724907
  4. [6]Abellán A, Desfilis E, Medina L, Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken. Front. Neuroanat 8, 59 (2014). 25071464 PMC4082316
  5. [7]Montagnese CM, Krebs JR, Meyer G, The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: A Golgi study. Cell Tissue Res. 283, 263– 282 (1996). 8593656
  6. [8]Naumann RK, Ondracek JM, Reiter S, Shein-Idelson M, Tosches MA, Yamawaki TM, Laurent G, The reptilian brain. Curr. Biol 25, R317– R321 (2015). 25898097 PMC4406946
  7. [9]Striedter GF, Evolution of the hippocampus in reptiles and birds. J. Comp. Neurol 524, 496– 517 (2016). 25982694
  8. [10]O’Keefe J, Dostrovsky J, The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171– 175 (1971). 5124915
  9. [11]O’Keefe J, Nadel L, The hippocampus as a cognitive map (Oxford University Press, Oxford, 1978).
  10. [12]Buzsáki G, Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus. 25, 1073– 1188 (2015). 26135716 PMC4648295
  11. [13]Buzsáki G, Moser EI, Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci 16, 130– 138 (2013). 23354386 PMC4079500
  12. [14]Sherry DF, Grella SL, Guigueno MF, White DJ, Marrone DF, Are there place cells in the avian hippocampus? Brain. Behav. Evol 90, 73– 80 (2017). 28866682
  13. [15]Kahn MC, Siegel JJ, Jechura TJ, Bingman VP, Response properties of avian hippocampal formation cells in an environment with unstable goal locations. Behav. Brain Res 191, 153– 163 (2008). 18468703
  14. [18]Ben-Yishay E, Krivoruchko K, Ron S, Ulanovsky N, Derdikman D, Gutfreund Y, Directional tuning in the hippocampal formation of birds. Curr. Biol, 1– 11 (2021). 33974847
  15. [20]Norimoto H, Fenk LA, Li HH, Tosches MA, Gallego-Flores T, Hain D, Reiter S, Kobayashi R, Macias A, Arends A, Klinkmann M, Laurent G, A claustrum in reptiles and its role in slow-wave sleep. Nature. 578, 413– 418 (2020). 32051589
  16. [21]Yeganegi H, Luksch H, Ondracek JM, Hippocampal-like network dynamics underlie avian sharp wave-ripples. bioRxiv (2019), doi: 10.1101/825075. · DOI
  17. [22]Rattenborg NC, Martinez-Gonzalez D, Roth TC, Pravosudov VV, Hippocampal memory consolidation during sleep: A comparison of mammals and birds. Biol. Rev 86, 658– 691 (2011). 21070585 PMC3117012
  18. [23]Killian NJ, Jutras MJ, Buffalo EA, A map of visual space in the primate entorhinal cortex. Nature. 491, 761– 764 (2012). 23103863 PMC3565234
  19. [24]Yartsev MM, Ulanovsky N, Representation of three-dimensional space in the hippocampus of flying bats. Science. 340, 367– 372 (2013). 23599496
  20. [26]Sherry DF, Vaccarino AL, Buckenham K, Herz R, The hippocampal complex of food-storing birds. Brain Behav Evol (1989). 2611638
  21. [27]Muller RU, Kubie JL, The firing of hippocampal place cells predicts the future position of freely moving rats. J. Neurosci 9, 4101– 4110 (1989). 2592993 PMC6569642
  22. [28]Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G, Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci 19, 274– 287 (1999). 9870957 PMC6782375
  23. [30]Muller RU, Bostock E, Taube JS, Kubie JL, On the directional firing properties of hippocampal place cells. J. Neurosci 14, 7235– 51 (1994). 7996172 PMC6576887
  24. [31]Atoji Y, Wild JM, Anatomy of the avian hippocampal formation. Rev. Neurosci 17, 3– 15 (2006). 16703939
  25. [32]Jung MW, Wiener SI, McNaughton BL, Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci 14, 7347– 7356 (1994). 7996180 PMC6576902
  26. [33]Smulders TV, The avian hippocampal formation and the stress response. Brain. Behav. Evol 90, 81– 91 (2017). 28866683
  27. [34]Patel J, Schomburg EW, Berényi A, Fujisawa S, Buzsáki G, Local generation and propagation of ripples along the septotemporal axis of the hippocampus. J. Neurosci 33, 17029– 17041 (2013). 24155307 PMC3807028
  28. [35]Yartsev MM, Witter MP, Ulanovsky N, Grid cells without theta oscillations in the entorhinal cortex of bats. Nature. 479, 103– 107 (2011). 22051680
  29. [36]Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsáki G, Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: Network and intracellular mechanisms. J. Neurosci 15, 30– 46 (1995). 7823136 PMC6578299
  30. [37]Moser EI, Kropff E, Moser M-B, Place cells, grid cells, and the brain’s spatial representation system. Annu. Rev. Neurosci 31, 69– 89 (2008). 18284371
  31. [39]Tömböl T, Davies DC, Németh A, Sebestény T, Alpár A, A comparative Golgi study of chicken (Gallus domesticus) and homing pigeon (Columba livia) hippocampus. Anat. Embryol. (Berl). 201, 85– 101 (2000). 10672361
  32. [40]Valero M, Cid E, Averkin RG, Aguilar J, Sanchez-Aguilera A, Viney TJ, Gomez-Dominguez D, Bellistri E, De La Prida LM, Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples. Nat. Neurosci 18, 1281– 1290 (2015). 26214372 PMC4820637
  33. [41]Montagnese CM, Krebs JR, Székely AD, Csillag A, A subpopulation of large calbindin-like immunopositive neurones is present in the hippocampal formation in food-storing but not in non-storing species of bird. Brain Res. 614, 291– 300 (1993). 8348321
  34. [42]Skaggs WE, McNaughton BL, Computational approaches to hippocampal function. Curr. Biol 2, 198 (1992). 1638156
  35. [43]Fiete IR, Hahnloser RHR, Fee MS, Seung HS, Temporal sparseness of the premotor drive is important for rapid learning in a neural network model of birdsong. J. Neurophysiol 92, 2274– 2282 (2004). 15071087
  36. [45]Danjo T, Toyoizumi T, Fujisawa S, Spatial representations of self and other in the hippocampus. Science. 359, 213– 218 (2018). 29326273
  37. [46]Radvansky BA, Dombeck DA, An olfactory virtual reality system for mice. Nat. Commun 9, 1– 14 (2018). 29483530 PMC5827522
  38. [47]Tavares RM, Mendelsohn A, Grossman Y, Williams CH, Shapiro M, Trope Y, Schiller D, A map for social navigation in the human brain. Neuron. 87, 231– 243 (2015). 26139376 PMC4662863
  39. [48]Calabrese E, Badea A, Watson C, Johnson GA, A quantitative magnetic resonance histology atlas of postnatal rat brain development with regional estimates of growth and variability. Neuroimage. 71, 196– 206 (2013). 23353030 PMC3639493

Cited by

Sorted by citations

Authors
Payne, H. L., Lynch, G. F., & Aronov, D.
Affiliations
  • Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
  • McGovern Institute for Brain Research (US)
Corresponding author
Aronov, D.
ORCID
Venue
Science
Publisher
American Association for the Advancement of Science (AAAS)
Published
2021-07-16
Volume
373
Issue
6552
Pages
343-348
ISSN
  • 0036-8075 (ISSN-L)
  • 1095-9203
DOI
10.1126/science.abg2009
PMC
PMC8503942
OpenAlex
W3182925168
Cited by
163
References
9
Citations by year
2026: 16 · 2025: 50 · 2024: 29 · 2023: 21 · 2022: 31 · 2021: 15 · 2020: 1
FWCI
12.88
Type
journal article
Language
en
Open access
Locations
  • Science (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (DP2 AG071918-01)
  • Arnold and Mabel Beckman Foundation (Beckman Young Investigator Award)
  • New York Stem Cell Foundation (Robertson Neuroscience Investigator Award)
  • Helen Hay Whitney Foundation
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
hippocampus, spatial memory, place cells, sharp-wave ripples, food caching, avian hippocampus, comparative neuroanatomy, vertebrate evolution
MeSH terms
Place Cells, Action Potentials, Animals, Feeding Behavior, Female, Hippocampus, Male, Neural Pathways, Neurons, Sleep, Passeriformes, Finches, Electrophysiological Phenomena, Spatial Memory

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