Path integration is thought to rely on vestibular and proprioceptive cues yet most studies in humans involve primarily visual input, providing limited insight into their respective contributions. We developed a paradigm involving walking in an omnidirectional treadmill in which participants were guided on two sides of a triangle and then found their back way to origin. In Experiment 1, we tested a range of different triangle types while keeping the distance of the unguided side constant to determine the influence of spatial geometry. Participants overshot the angle they needed to turn and undershot the distance they needed to walk, with no consistent effect of triangle type. In Experiment 2, we manipulated distance while keeping angle constant to determine how path integration operated over both shorter and longer distances. Participants underestimated the distance they needed to walk to the origin, with error increasing as a function of the walked distance. To attempt to account for our findings, we developed configural-based computational models involving vector addition, the second of which included terms for the influence of past trials on the current one. We compared against a previously developed configural model of human path integration, the Encoding-Error model. We found that the vector addition models captured the tendency of participants to under-encode guided sides of the triangles and an influence of past trials on current trials. Together, our findings expand our understanding of body-based contributions to human path integration, further suggesting the value of vector addition models in understanding these important components of human navigation.

3rd Faculty of Medicine Charles University Ruská Prague Czech Republic

Center for Neuroscience University of California Davis Davis California United States of America

Cognitive Science Program University of Arizona Tucson Arizona United States of America

Evelyn McKnight Brain Institute University of Arizona Tucson Arizona United States of America

Psychology Department University of Arizona Tucson Arizona United States of America

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Darwin C. Charles Darwin's natural selection: being the second part of his big species book written from 1856 to 1858: Cambridge University Press; 1856/1987.

Görner P. Die optische und kinästhetische Orientierung der Trichterspinne Agelena Labyrinthica (Cl.). Zeitschrift für vergleichende Physiologie. 1958;41(2):111–53. 10.1007/bf00345583 DOI

Lindauer M. Kompaßorientierung In: Autrum H, Bünning E, v. Frisch K, Hadorn E, Kühn A, Mayr E, et al., editors. Orientierung der Tiere / Animal Orientation: Symposium in Garmisch-Partenkirchen 17–21 9 1962. Berlin, Heidelberg: Springer Berlin Heidelberg; 1963. p. 158–81.

Mittelstaedt M-L, Mittelstaedt H. Homing by path integration in a mammal. Naturwissenschaften. 1980;67(11):566–7. 10.1007/bf00450672 DOI

Etienne AS. The Control of Short-Distance Homing in the Golden Hamster In: Ellen P, Thinus-Blanc C, editors. Cognitive Processes and Spatial Orientation in Animal and Man: Volume I Experimental Animal Psychology and Ethology. Dordrecht: Springer Netherlands; 1987. p. 233–51.

Alyan S, Jander R. Short-range homing in the house mouse, Mus musculus: stages in the learning of directions. Animal Behaviour. 1994;48(2):285–98.

Tolman EC. Cognitive maps in rats and men. Psychological Review. 1948;55(4):189–208. 10.1037/h0061626 PubMed DOI

Mittelstaedt H, Mittelstaedt M-L, editors. Homing by Path Integration1982; Berlin, Heidelberg: Springer Berlin Heidelberg.

Wehner R, Srinivasan MV. Searching Behavior of Desert Ants, Genus Cataglyphis (Formicidae, Hymenoptera). Journal of Comparative Physiology. 1981;142(3):315–38. WOS:A1981LT49400004.

Mittelstaedt H. The role of multimodal convergence in homing by path integration. Fortschritte der Zoologie. 1983;28:197–212.

Green J, Adachi A, Shah KK, Hirokawa JD, Magani PS, Maimon G. A neural circuit architecture for angular integration in Drosophila. Nature. 2017;546:101 10.1038/nature22343 PubMed DOI PMC

Seguinot V, Cattet J, Benhamou S. Path integration in dogs. Animal Behaviour. 1998;55(4):787–97. 10.1006/anbe.1997.0662 PubMed DOI

Herrick FH. Homing Powers of the Cat. The Scientific Monthly. 1922;14(6):525–39.

Beritashvili IS. Neural mechanisms of higher vertebrate behavior. 1965.

Redish AD. Beyond the Cognitive Map. Boston, MA: MIT Press; 1999.

Gallistel CR. The Organization of Learning. Cambridge, MA: MT Press; 1990.

Klatzky RL, Loomis JM, Golledge RG. Encoding spatial representations through nonvisually guided locomotion In: Medin, editor. The psychology of learning and motivation. 37: Academic Press; 1997.

Chance SS, Gaunet F, Beall AC, Loomis JM. Locomotion mode affects the updating of objects encountered during travel: The contribution of vestibular and proprioceptive inputs to path integration. Presence-Teleop Virt. 1998;7(2):168–78. 10.1162/105474698565659 WOS:000072949600006. DOI

Starrett MJ, Ekstrom AD. Perspective: Assessing the Flexible Acquisition, Integration, and Deployment of Human Spatial Representations and Information. Frontiers in human neuroscience. 2018;12. PubMed PMC

Taube JS, Valerio S, Yoder RM. Is Navigation in Virtual Reality with fMRI Really Navigation? Journal of Cognitive Neuroscience. 2013. Epub 2013/03/16. 10.1162/jocn_a_00386 . PubMed DOI PMC

Loomis JM, Klatzky RL, Golledge RG, Cicinelli JG, Pellegrino JW, Fry PA. Nonvisual navigation by blind and sighted: Assessment of path integration ability. Journal of Experimental Psychology: General. 1993;122(1):73–91. 10.1037/0096-3445.122.1.73 PubMed DOI

Müller M, Wehner R. Path integration in desert ants, Cataglyphis fortis. Proceedings of the National Academy of Sciences. 1988;85(14):5287–90. 10.1073/pnas.85.14.5287 PubMed DOI PMC

Cartwright BA, Collett TS. Landmark maps for honeybees. Biological Cybernetics. 1987;57(1):85–93. 10.1007/bf00318718 DOI

Etienne AS, Maurer R, Berlie J, Reverdin B, Rowe T, Georgakopoulos J, et al. Navigation through vector addition. Nature. 1998;396(6707):161–4. 10.1038/24151 PubMed DOI

Etienne AS, Maurer R, Seguinot V. Path integration in mammals and its interaction with visual landmarks. J Exp Biol. 1996;199(Pt 1):201–9. . PubMed

Kubie JL, Fenton AA. Heading-vector navigation based on head-direction cells and path integration. Hippocampus. 2009;19(5):456–79. 10.1002/hipo.20532 PubMed DOI

Wittmann T, Schwegler H. Path integration—a network model. Biological Cybernetics. 1995;73(6):569–75. 10.1007/bf00199549 DOI

Fujita N, Loomis JM, Klatzky RL, Golledge RG. A Minimal Representation for Dead-Reckoning Navigation: Updating the Homing Vector. Geographical Analysis. 1990;22(4):324–35. 10.1111/j.1538-4632.1990.tb00214.x DOI

Benhamou S, Séguinot V. How to find one's way in the labyrinth of path integration models. Journal of Theoretical Biology. 1995;174(4):463–6.

Etienne AS, Jeffery KJ. Path integration in mammals. Hippocampus. 2004;14(2):180–92. 10.1002/hipo.10173 PubMed DOI

Fujita N, Klatzky RL, Loomis JM, Golledge RG. The Encoding-Error Model of Pathway Completion without Vision. Geographical Analysis. 1993;25(4):295–314. 10.1111/j.1538-4632.1993.tb00300.x DOI

Klatzky RL, Beall AC, Loomis JM, Golledge RG, Philbeck JW. Human navigation ability: Tests of the encoding-error model of path integration. Spatial Cognition and Computation. 1999;1(1):31–65. 10.1023/a:1010061313300 DOI

Chrastil ER, Warren WH. Rotational error in path integration: encoding and execution errors in angle reproduction. Experimental Brain Research. 2017;235(6):1885–97. 10.1007/s00221-017-4910-y PubMed DOI

Wiener JM, Berthoz A, Wolbers T. Dissociable cognitive mechanisms underlying human path integration. Experimental Brain Research. 2011;208(1):61–71. 10.1007/s00221-010-2460-7 PubMed DOI

Klatzky RL, Loomis JM, Golledge RG, Cicinelli JG, Doherty S, Pellegrino JW. Acquisition of Route and Survey Knowledge in the Absence of Vision. Journal of Motor Behavior. 1990;22(1):19–43. 10.1080/00222895.1990.10735500 PubMed DOI

Petzschner FH, Glasauer S. Iterative Bayesian Estimation as an Explanation for Range and Regression Effects: A Study on Human Path Integration. The Journal of Neuroscience. 2011;31(47):17220–9. 10.1523/JNEUROSCI.2028-11.2011 PubMed DOI PMC

Teghtsoonian R, Teghtsoonian M. Range and regression effects in magnitude scaling. Perception & Psychophysics. 1978;24(4):305–14. 10.3758/bf03204247 PubMed DOI

Cheng K. A purely geometric module in the rat's spatial representation. Cognition. 1986;23(2):149–78. 10.1016/0010-0277(86)90041-7 PubMed DOI

Landau B, Gleitman H, Spelke E. Spatial knowledge and geometric representation in a child blind from birth. Science. 1981;213(4513):1275–8. 10.1126/science.7268438 PubMed DOI

Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature. 2005;436(7052):801 10.1038/nature03721 PubMed DOI

Bellmund JLS, Gärdenfors P, Moser EI, Doeller CF. Navigating cognition: Spatial codes for human thinking. Science. 2018;362(6415):eaat6766 10.1126/science.aat6766 PubMed DOI

Milivojevic B, Doeller CF. Mnemonic networks in the hippocampal formation: From spatial maps to temporal and conceptual codes. Journal of Experimental Psychology: General. 2013;142(4):1231. PubMed

Chen X, He Q, Kelly Jonathan W, Fiete Ila R, McNamara Timothy P. Bias in Human Path Integration Is Predicted by Properties of Grid Cells. Current Biology. 2015;25(13):1771–6. 10.1016/j.cub.2015.05.031 PubMed DOI

Moser EI, Moser M-B. A metric for space. Hippocampus. 2008;18(12):1142–56. 10.1002/hipo.20483 PubMed DOI

Cheung A, Ball D, Milford M, Wueth G, Wiles J. Maintaining a Cognitive Map in Darkness: The Need to Fuse Boundary Knowledge with Path Integration. PLoS Comput Biol. 2012;8(8):1–22. PubMed PMC

Burak Y, Fiete IR. Accurate Path Integration in Continuous Attractor Network Models of Grid Cells. PLOS Computational Biology. 2009;5(2):e1000291 10.1371/journal.pcbi.1000291 PubMed DOI PMC

Palminteri S, Wyart V, Koechlin E. The Importance of Falsification in Computational Cognitive Modeling. Trends in Cognitive Sciences. 2017;21(6):425–33. 10.1016/j.tics.2017.03.011 PubMed DOI

Wilson RC, Collins AGE. Ten simple rules for the computational modeling of behavioral data. eLife. 2019;8:e49547 10.7554/eLife.49547 PubMed DOI PMC

Stevens SS. Psychophysics: introduction to its perceptual, neural, and social prospects. New York,: Wiley; 1975. v, 329 p. p.

Philbeck JW, Klatzky RL, Behrmann M, Loomis JM, Goodridge J. Active control of locomotion facilitates nonvisual navigation. J Exp Psychol Hum Percept Perform. 2001;27(1):141–53. . PubMed

Yamamoto N, Philbeck JW, Woods AJ, Gajewski DA, Arthur JC, Potolicchio SJ, et al. Medial Temporal Lobe Roles in Human Path Integration. Plos One. 2014;9(5). ARTN e9658310.1371/journal.pone.0096583. WOS:000338029800088. PubMed PMC

Carriot J, Jamali M, Brooks JX, Cullen KE. Integration of Canal and Otolith Inputs by Central Vestibular Neurons Is Subadditive for Both Active and Passive Self-Motion: Implication for Perception. The Journal of Neuroscience. 2015;35(8):3555–65. 10.1523/JNEUROSCI.3540-14.2015 PubMed DOI PMC

Moar I, Bower GH. Inconsistency in Spatial Knowledge. Memory & Cognition. 1983;11(2):107–13. 10.3758/Bf03213464 WOS:A1983QM26800001. PubMed DOI

Chrastil ER, Sherrill KR, Hasselmo ME, Stern CE. There and Back Again: Hippocampus and Retrosplenial Cortex Track Homing Distance during Human Path Integration. Journal of Neuroscience. 2015;35(46):15442–52. 10.1523/JNEUROSCI.1209-15.2015 WOS:000366054500020. PubMed DOI PMC

Marchette SA, Bakker A, Shelton AL. Cognitive Mappers to Creatures of Habit: Differential Engagement of Place and Response Learning Mechanisms Predicts Human Navigational Behavior. The Journal of Neuroscience. 2011;31(43):15264–8. 10.1523/JNEUROSCI.3634-11.2011 PubMed DOI PMC

Weisberg SM, Schinazi VR, Newcombe NS, Shipley TF, Epstein RA. Variations in cognitive maps: understanding individual differences in navigation. J Exp Psychol Learn Mem Cogn. 2014;40(3):669–82. Epub 2013/12/25. 10.1037/a0035261 . PubMed DOI

Dillon MR, Huang Y, Spelke ES. Core foundations of abstract geometry. Proceedings of the National Academy of Sciences. 2013;110(35):14191–5. 10.1073/pnas.1312640110 PubMed DOI PMC

Lee SA, Sovrano VA, Spelke ES. Navigation as a source of geometric knowledge: Young children’s use of length, angle, distance, and direction in a reorientation task. Cognition. 2012;123(1):144–61. 10.1016/j.cognition.2011.12.015 PubMed DOI PMC

Wan X, Wang RF, Crowell JA. Effects of Basic Path Properties on Human Path Integration. Spatial Cognition & Computation. 2013;13(1):79–101. 10.1080/13875868.2012.678521 DOI

Chadwick MJ, Jolly AEJ, Amos DP, Hassabis D, Spiers HJ. A Goal Direction Signal in the Human Entorhinal/Subicular Region. Current Biology. 2015;25(1):87–92. 10.1016/j.cub.2014.11.001 WOS:000347409900031. PubMed DOI PMC

Lackner JR, DiZio P. Vestibular, proprioceptive, and haptic contributions to spatial orientation. Annu Rev Psychol. 2005;56:115–47. 10.1146/annurev.psych.55.090902.142023 PubMed DOI

Loomis JM, Beall AC. Visually controlled locomotion: Its dependence on optic flow, three-dimensional space perception, and cognition. Ecol Psychol. 1998;10(3–4):271–85. 10.1207/s15326969eco103&4_6 WOS:000077500700006. DOI

Matthis JS, Yates JL, Hayhoe MM. Gaze and the Control of Foot Placement When Walking in Natural Terrain. Current Biology. 2018;28(8):1224–+. 10.1016/j.cub.2018.03.008 WOS:000430694900043. PubMed DOI PMC

Visell Y, Giordano BL, Millet G, Cooperstock JR. Vibration Influences Haptic Perception of Surface Compliance During Walking. Plos One. 2011;6(3). ARTN e1769710.1371/journal.pone.0017697. WOS:000288813900006. PubMed PMC

Souman JL, Giordano PR, Schwaiger M, Frissen I, Thümmel T, Ulbrich H, et al. CyberWalk: Enabling unconstrained omnidirectional walking through virtual environments. ACM Transactions on Applied Perception (TAP). 2011;8(4):25.

Waller D, Loomis JM, Haun DBM. Body-based senses enhance knowledge of directions in large-scale environments. Psychon B Rev. 2004;11(1):157–63. 10.3758/Bf03206476 ISI:000220674200022. PubMed DOI

Warren WH. Non-Euclidean navigation. The Journal of Experimental Biology. 2019;222(Suppl 1):jeb187971 10.1242/jeb.187971 PubMed DOI

Keung W, Hagen TA, Wilson RC. Regulation of evidence accumulation by pupil-linked arousal processes. Nature Human Behaviour. 2019;3(6):636–45. 10.1038/s41562-019-0551-4 PubMed DOI

Lau B, Glimcher PW. Dynamic response-by-response models of matching behavior in rhesus monkeys. J Exp Anal Behav. 2005;84(3):555–79. 10.1901/jeab.2005.110-04 . PubMed DOI PMC

Schwarz G. Estimating the Dimension of a Model. Ann Statist. 1978;6(2):461–4. 10.1214/aos/1176344136 DOI

Akaike H. A new look at the statistical model identification. IEEE Transactions on Automatic Control. 1974;19(6):716–23. 10.1109/TAC.1974.1100705 DOI

Rigoux L, Stephan KE, Friston KJ, Daunizeau J. Bayesian model selection for group studies—revisited. Neuroimage. 2014;84:971–85. Epub 2013/09/11. 10.1016/j.neuroimage.2013.08.065 . PubMed DOI

Rouder JN, Speckman PL, Sun DC, Morey RD, Iverson G. Bayesian t tests for accepting and rejecting the null hypothesis. Psychon B Rev. 2009;16(2):225–37. 10.3758/Pbr.16.2.225 WOS:000264915700001. PubMed DOI

Yamamoto N, Philbeck JW. Intrinsic frames of reference in haptic spatial learning. Cognition. 2013;129(2):447–56. 10.1016/j.cognition.2013.08.011 WOS:000327368500023. PubMed DOI