Science - USA (2021-07-09)

5. J. O’Keefe, J. Dostrovsky,Brain Res. 34 , 171–175 (1971).


6. E. I. Moser, M. B. Moser, B. L. McNaughton,Nat. Neurosci. 20 ,
   1448 – 1464 (2017).


7. R. M. Grieveset al.,Nat. Commun. 11 , 789 (2020).


8. M. M. Yartsev, N. Ulanovsky,Science 340 , 367–372 (2013).


9. M. Geva-Sagiv, S. Romani, L. Las, N. Ulanovsky,Nat. Neurosci.
   19 , 952–958 (2016).


10. M. J. Wohlgemuth, C. Yu, C. F. Moss,Front. Cell. Neurosci. 12 ,
    270 (2018).


11. Nonlocal positional coding has also been observed in awake,
    stationary animals before and after spatial exploration
    and at decision points ( 12 – 15 ).


12. D. J. Foster, M. A. Wilson,Nature 440 , 680–683 (2006).


13. K. Diba, G. Buzsáki,Nat. Neurosci. 10 , 1241–1242 (2007).


14. A. Johnson, A. D. Redish,J. Neurosci. 27 , 12176– 12189
    (2007).


15. A. D. Redish,Nat. Rev. Neurosci. 17 , 147–159 (2016).


16. J. O’Keefe, M. L. Recce,Hippocampus 3 , 317–330 (1993).


17. W. E. Skaggs, B. L. McNaughton, M. A. Wilson, C. A. Barnes,
    Hippocampus 6 , 149–172 (1996).


18. G. Buzsáki,Neuron 33 , 325–340 (2002).


19. G. Buzsáki,Hippocampus 15 , 827–840 (2005).


20. R. L. Buckner,Annu. Rev. Psychol. 61 , 27–48, C1–C8 (2010).


21. A. S. Gupta, M. A. A. van der Meer, D. S. Touretzky,
    A. D. Redish,Nat. Neurosci. 15 , 1032–1039 (2012).


22. T. Eliavet al.,Cell 175 , 1119–1130.e15 (2018).


23. M. Wang, D. J. Foster, B. E. Pfeiffer,Science 370 , 247– 250
    (2020).


24. K. Kayet al.,Cell 180 , 552–567.e25 (2020).


25. E. R. Wood, P. A. Dudchenko, R. J. Robitsek, H. Eichenbaum,
    Neuron 27 , 623–633 (2000).


26. L. M. Frank, E. N. Brown, M. Wilson,Neuron 27 , 169–178 (2000).
    27. J. Ferbinteanu, M. L. Shapiro,Neuron 40 , 1227– 1239
    (2003).
    28. R. U. Muller, J. L. Kubie,J. Neurosci. 9 , 4101–4110 (1989).
    29. F. P. Battaglia, G. R. Sutherland, B. L. McNaughton,J. Neurosci.
    24 , 4541–4550 (2004).
    30. The average flight speed of a bat is ~3 m/s, with peak speeds
    up to ~6 m/s under laboratory conditions.
    31. D. Genzel, M. M. Yartsev,J. Neurosci. Methods 348 , 108970
    (2021).
    32. A. Sarel, A. Finkelstein, L. Las, N. Ulanovsky,Science 355 ,
    176 – 180 (2017).
    33. D. B. Omer, S. R. Maimon, L. Las, N. Ulanovsky,Science 359 ,
    218 – 224 (2018).
    34. C. G. Kentros, N. T. Agnihotri, S. Streater, R. D. Hawkins,
    E. R. Kandel,Neuron 42 , 283–295 (2004).
    35. L. Meshulam, J. L. Gauthier, C. D. Brody, D. W. Tank, W. Bialek,
    Neuron 96 , 1178–1191.e4 (2017).
    36. F. Stefaniniet al.,Neuron 107 , 703–716.e4 (2020).
    37. G. E. Hough, V. P. Bingman,J. Comp. Physiol. A Neuroethol.
    Sens. Neural Behav. Physiol. 190 , 1047–1062 (2004).
    38. H. S. Courelliset al.,PLOS Biol. 17 , e3000546 (2019).
    39. E. Vinepinskyet al.,Sci. Rep. 10 , 14762 (2020).
    40. K. L. Stachenfeld, M. M. Botvinick, S. J. Gershman,Nat. Neurosci.
    20 , 1643–1653 (2017).
    41. M. M. Yartsev,Science 358 , 466–469 (2017).
    42. S. R. Datta, D. J. Anderson, K. Branson, P. Perona, A. Leifer,
    Neuron 104 , 11–24 (2019).

ACKNOWLEDGMENTS

We thank O. Tchernichovski for extensive discussion of the results,

comments on the manuscript, and help with analysis; D. Foster

for discussion of the results and manuscript; J. Widloski, K. Kay,

and D. Foster for helpful discussions on a revised version of

the manuscript; L. Kang, A. Forli, W. Liberti, T. Schmid, B. Styr, and

M. Snyder for careful reading and comments on the manuscript;

members of the Yartsev laboratory for discussion and comments;

D. Genzel for assistance with the design of the experimental

task and training protocols; Y. Minton and L. Loomis for experimental

room maintenance and animal care; and G. Lawson and the staff of

the Office of Laboratory Animal Care for support with animal

husbandry and care.Funding:This work was supported by

the New York Stem Cell Foundation (NYSCF-RNI40), the Air Force

Office of Scientific Research (FA9550-17-1-0412), the Office of

Naval Research (N00014-21-1-2063), the Packard Fellowship

(2017-66825), the National Institute of Neurological Disorders and

Stroke (R01NS118422-01), the Valle Foundation (VS-2020-34),

and the Searle Scholars Program (SSP-2016-1412) to M.M.Y.

Author contributions:N.M.D. and M.M.Y. designed the research,

analyzed the data, and wrote the manuscript. N.M.D. performed

the experiments.Competing interests:The authors declare no

competing interests.Data and materials availability:All data are

available in the main text or the supplementary materials.

SUPPLEMENTARY MATERIALS

science.sciencemag.org/content/373/6551/242/suppl/DC1

Materials and Methods

Figs. S1 to S15

References ( 43 – 54 )

MDAR Reproducibility Checklist

11 December 2020; accepted 1 June 2021

10.1126/science.abg1278

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