Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-22T12:36:20.760Z Has data issue: false hasContentIssue false
  • English
  • Français

Navigating in a three-dimensional world

Published online by Cambridge University Press:  08 October 2013

Kathryn J. Jeffery ,
Aleksandar Jovalekic ,
Madeleine Verriotis  and
Robin Hayman
Kathryn J. Jeffery
Affiliation:
Department of Cognitive, Perceptual and Brain Sciences, Division of Psychology & Language Sciences, University College London, London WC1H 0AP, United Kingdom. [email protected]/jefferylab/
Aleksandar Jovalekic
Affiliation:
Institute of Neuroinformatics, University of Zurich, CH-8057 Zurich, Switzerland. [email protected]
Madeleine Verriotis
Affiliation:
Department of Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, United Kingdom. [email protected]
Robin Hayman
Affiliation:
Institute of Cognitive Neuroscience, Alexandra House, London WC1N 3AR, United Kingdom. [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The study of spatial cognition has provided considerable insight into how animals (including humans) navigate on the horizontal plane. However, the real world is three-dimensional, having a complex topography including both horizontal and vertical features, which presents additional challenges for representation and navigation. The present article reviews the emerging behavioral and neurobiological literature on spatial cognition in non-horizontal environments. We suggest that three-dimensional spaces are represented in a quasi-planar fashion, with space in the plane of locomotion being computed separately and represented differently from space in the orthogonal axis – a representational structure we have termed “bicoded.” We argue that the mammalian spatial representation in surface-travelling animals comprises a mosaic of these locally planar fragments, rather than a fully integrated volumetric map. More generally, this may be true even for species that can move freely in all three dimensions, such as birds and fish. We outline the evidence supporting this view, together with the adaptive advantages of such a scheme.

Keywords

ethologygrid cellshead direction cellshippocampusnavigationneural encodingplace cellsspatial cognitionthree-dimensional
Type
Target Article
Information
Behavioral and Brain Sciences , Volume 36 , Issue 5 , October 2013 , pp. 523 - 543
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aflalo, T. N. & Graziano, M. S. (2008) Four-dimensional spatial reasoning in humans. Journal of Experimental Psychology: Human Perception and Performance 34(5):1066–77.Google Scholar
Angelaki, D. E. & Cullen, K. E. (2008) Vestibular system: The many facets of a multimodal sense. Annual Review of Neuroscience 31:125–50.Google Scholar
Angelaki, D. E., McHenry, M. Q., Dickman, J. D., Newlands, S. D. & Hess, B. J. (1999) Computation of inertial motion: Neural strategies to resolve ambiguous otolith information. Journal of Neuroscience 19(1):316–27.Google Scholar
Aoki, H., Ohno, R. & Yamaguchi, T. (2005) The effect of the configuration and the interior design of a virtual weightless space station on human spatial orientation. Acta Astronautica 56:1005–16.Google Scholar
Bardunias, P. M. & Jander, R. (2000) Three dimensional path integration in the house mouse (Mus domestica). Naturwissenschaften 87(12):532–34.Google Scholar
Barry, C., Hayman, R., Burgess, N. & Jeffery, K. J. (2007) Experience-dependent rescaling of entorhinal grids. Nature Neuroscience 10(6):682–84.Google Scholar
Bhalla, M. & Proffitt, D. R. (1999) Visual-motor recalibration in geographical slant perception. Journal of Experimental Psychology: Human Perception and Performance 25(4):1076–96.Google Scholar
Brill, R., Lutcavage, M., Metzger, G., Stallings, J., Bushnell, P., Arendt, M., Lucy, J., Watson, C. & Foley, D. (2012) Horizontal and vertical movements of juvenile North Atlantic Bluefin Tuna (Thunnus thynnus) in the western North Atlantic determined using ultrasonic telemetry, with reference to population assessment by aerial surveys. Fortschritte der Zoologie 100:155–67.Google Scholar
Brown, M. F. & Lesniak-Karpiak, K. B. (1993) Choice criterion effects in the radial-arm maze – Maze-arm incline and brightness. Learning and Motivation 24(1):23–39.Google Scholar
Büchner, S., Hölscher, C. & Strube, G. (2007) Path choice heuristics for navigation related to mental representations of a building. In: Proceedings of the 2nd European Cognitive Science Conference, Delphi, Greece, 23–27 May, 2007, ed. Vosniadou, S., Kayser, D. & Protopapas, A., pp. 504–509. Erlbaum/Taylor & Francis.Google Scholar
Burt de Perera, T., de Vos, A. & Guilford, T. (2005) The vertical component of a fish's spatial map. Animal Behaviour 70:405–409.Google Scholar
Calton, J. L. & Taube, J. S. (2005) Degradation of head direction cell activity during inverted locomotion. Journal of Neuroscience 25(9):2420–28.Google Scholar
Carey, F. G. (1992) Through the thermocline and back again. Oceanus 35:79–85.Google Scholar
Creem, S. H. & Proffitt, D. R. (1998) Two memories for geographical slant: Separation and interdependence of action and awareness. Psychonomic Bulletin and Review 5(1):22–36.Google Scholar
Creem, S. H. & Proffitt, D. R. (2001) Defining the cortical visual systems: “What,” “where,” and “how.” Acta Psychologica (Amsterdam) 107(1–3):43–68.Google Scholar
Dacke, M. & Srinivasan, M. V. (2007) Honeybee navigation: Distance estimation in the third dimension. Journal of Experimental Biology 210(Pt. 5):845–53.Google Scholar
Dudchenko, P. A. & Zinyuk, L. E. (2005) The formation of cognitive maps of adjacent environments: Evidence from the head direction cell system. Behavioral Neuroscience 119(6):1511–23.Google Scholar
Durgin, F. H., Hajnal, A., Li, Z., Tonge, N. & Stigliani, A. (2011) An imputed dissociation might be an artifact: Further evidence for the generalizability of the observations of Durgin et al. 2010. Acta Psychologica (Amsterdam) 138(2):281–84.Google Scholar
Durgin, F. H., Klein, B., Spiegel, A., Strawser, C. J. & Williams, M. (2012) The social psychology of perception experiments: Hills, backpacks, glucose and the problem of generalizability. Journal of Experimental Psychology: Human Perception and Performance 2012; 38(6):1582–95.Google Scholar
Durgin, F. H. & Li, Z. (2011) Perceptual scale expansion: An efficient angular coding strategy for locomotor space. Attention, Perception, and Psychophysics 73(6):1856–70.Google Scholar
Esch, H. E. & Burns, J. E. (1995) Honeybees use optic flow to measure the distance of a food source. Naturwissenschaften 82:38–40.Google Scholar
Etienne, A. S. & Jeffery, K. J. (2004) Path integration in mammals. Hippocampus 14:180–92.Google Scholar
Fenton, A. A., Kao, H. Y., Neymotin, S. A., Olypher, A., Vayntrub, Y., Lytton, W. W. & Ludvig, N. (2008) Unmasking the CA1 ensemble place code by exposures to small and large environments: More place cells and multiple, irregularly arranged, and expanded place fields in the larger space. Journal of Neuroscience 28(44):11250–62.Google Scholar
Garling, T., Anders, B., Lindberg, E. & Arce, C. (1990) Is elevation encoded in cognitive maps? Journal of Environmental Psychology 10:341–51.Google Scholar
Gibson, J. J. & Cornsweet, J. (1952) The perceived slant of visual surfaces – Optical and geographical. Journal of Experimental Psychology 44(1):11–15.Google Scholar
Goodridge, J. P., Dudchenko, P. A., Worboys, K. A., Golob, E. J. & Taube, J. S. (1998) Cue control and head direction cells. Behavioral Neuroscience 112(4):749–61.Google Scholar
Grah, G., Wehner, R. & Ronacher, B. (2007) Desert ants do not acquire and use a three-dimensional global vector. Frontiers in Zoology 4:12.Google Scholar
Grobéty, M. C. & Schenk, F. (1992a) Spatial learning in a three-dimensional maze. Animal Behaviour 43(6):1011–20.Google Scholar
Grobéty, M.-C. & Schenk, F. (1992b) The influence of spatial irregularity upon radial-maze performance in the rat. Animal Learning and Behavior 20(4):393–400.Google Scholar
Hafting, T., Fyhn, M., Molden, S., Moser, M. B. & Moser, E. I. (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806.Google Scholar
Hayman, R., Verriotis, M. A., Jovalekic, A., Fenton, A. A. & Jeffery, K. J. (2011) Anisotropic encoding of three-dimensional space by place cells and grid cells. Nature Neuroscience 14(9):1182–88.Google Scholar
Henderson, J., Hurly, T. A. & Healy, S. D. (2001) Rufous hummingbirds' memory for flower location. Animal Behaviour 61(5):981–86.Google Scholar
Henderson, J., Hurly, T. A. & Healy, S. D. (2006) Spatial relational learning in rufous hummingbirds (Selasphorus rufus). Animal Cognition 9:201–205.Google Scholar
Hess, D., Koch, J. & Ronacher, B. (2009) Desert ants do not rely on sky compass information for the perception of inclined path segments. Journal of Experimental Biology 212(10):1528–34.Google Scholar
Holbrook, R. I. & Burt de Perera, T. B. (2009) Separate encoding of vertical and horizontal components of space during orientation in fish. Animal Behaviour 78(2):241–45.Google Scholar
Holbrook, R. I. & Burt de Perera, T. (2011a) Fish navigation in the vertical dimension: Can fish use hydrostatic pressure to determine depth? Fish and Fisheries 12(4):370–379.Google Scholar
Hölscher, C., Meilinger, T., Vrachliotis, G., Brösamle, M. & Knauff, M. (2006) Up the down staircase: Wayfinding strategies and multi-level buildings. Journal of Environmental Psychology 26(4):284–99.Google Scholar
Jeffery, K. J. (2007) Integration of the sensory inputs to place cells: What, where, why, and how? Hippocampus 17(9):775–85.Google Scholar
Jeffery, K. J., Anand, R. L. & Anderson, M. I. (2006) A role for terrain slope in orienting hippocampal place fields. Experimental Brain Research 169(2):218–25.Google Scholar
Jeffery, K. J. & Burgess, N. (2006) A metric for the cognitive map – Found at last? Trends in Cognitive Sciences 10(1):1–3.Google Scholar
Jovalekic, A., Hayman, R., Becares, N., Reid, H., Thomas, G., Wilson, J. & Jeffery, K. (2011) Horizontal biases in rats' use of three-dimensional space. Behavioural Brain Research 222(2):279–88.Google Scholar
Kammann, R. (1967) The overestimation of vertical distance and its role in the moon illusion. Attention, Perception, and Psychophysics 2(12):585–89.Google Scholar
Kelly, J. (2011) Head for the hills: The influence of environmental slant on spatial memory organization. Psychonomic Bulletin and Review 18(4):774–80.Google Scholar
Knierim, J. J. & McNaughton, B. L. (2001) Hippocampal place-cell firing during movement in three-dimensional space. Journal of Neurophysiology 85(1):105–16.Google Scholar
Knierim, J. J., McNaughton, B. L. & Poe, G. R. (2000) Three-dimensional spatial selectivity of hippocampal neurons during space flight. Nature Neuroscience 3(3):209–10.Google Scholar
Knierim, J. J., Poe, G. R. & McNaughton, B. L. (2003) Ensemble neural coding of place in zero-g. In: The Neurolab Spacelab Mission: Neuroscience research in space. Results from the STS-90, Neurolab Spacelab Mission, NASA Report SP-2003–535, ed. Buckey, J. C. Jr. & Homick, J. L., pp. 63–68. NASA.Google Scholar
Lackner, J. R. & Graybiel, A. (1983) Perceived orientation in free-fall depends on visual, postural, and architectural factors. Aviation, Space, and Environmental Medicine 54(1):47–51.Google Scholar
Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M. B. & Moser, E. I. (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305(5688):1295–98.Google Scholar
Li, Z. & Durgin, F. H. (2009) Downhill slopes look shallower from the edge. Journal of Vision 9(11):6–15.Google Scholar
Li, Z. & Durgin, F. H. (2010) Perceived slant of binocularly viewed large-scale surfaces: A common model from explicit and implicit measures. Journal of Vision 10(14):article 13:1–16.Google Scholar
Loomis, J. M., Da Silva, J. A., Fujita, N. & Fukusima, S. S. (1992) Visual space perception and visually directed action. Journal of Experimental Psychology: Human Perception and Performance 18(4):906–921.Google Scholar
Merfeld, D. M., Young, L. R., Oman, C. M. & Shelhamer, M. J. (1993) A multidimensional model of the effect of gravity on the spatial orientation of the monkey. Journal of Vestibular Research 3(2):141–61.Google Scholar
Merfeld, D. M. & Zupan, L. H. (2002) Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. Journal of Neurophysiology 87(2):819–33.Google Scholar
Mittelstaedt, H. (1998) Origin and processing of postural information. Neuroscience and Biobehavioral Reviews 22(4):473–78.Google Scholar
Moghaddam, M., Kaminsky, Y. L., Zahalka, A. & Bures, J. (1996) Vestibular navigation directed by the slope of terrain. Proceedings of the National Academy of Sciences of the United States of America 93(8):3439–43.Google Scholar
Montello, D. R. & Pick, H. L. (1993) Integrating knowledge of vertically aligned large-scale spaces. Environment and Behavior 25(3):457–84.Google Scholar
Moser, E. I., Kropff, E. & Moser, M. B. (2008) Place cells, grid cells, and the brain's spatial representation system. Annual Review of Neuroscience 31:69–89.Google Scholar
Moser, E. I. & Moser, M. B. (2008) A metric for space. Hippocampus 18(12):1142–56.Google Scholar
Nardi, D. & Bingman, V. P. (2009b) Slope-based encoding of a goal location is unaffected by hippocampal lesions in homing pigeons (Columba livia). Behavioural Brain Research 205(1):322–26.Google Scholar
Nardi, D., Newcombe, N. S. & Shipley, T. F. (2011) The world is not flat: Can people reorient using slope? Journal of Experimental Psychology. Learning, Memory and Cognition 37(2):354–67.Google Scholar
Nardi, D., Nitsch, K. P. & Bingman, V. P. (2010) Slope-driven goal location behavior in pigeons. Journal of Experimental Psychology. Animal Behavior Processes 36(4):430–42.Google Scholar
Nieh, J. C., Contrera, F. A. & Nogueira-Neto, P. (2003) Pulsed mass recruitment by a stingless bee, Trigona hyalinata . Proceedings of the Royal Society of London, B: Biological Sciences 270(1529):2191–96.Google Scholar
Nieh, J. C. & Roubik, D. W. (1998) Potential mechanisms for the communication of height and distance by a stingless bee, Melipona panamica. Behavioral Ecology and Sociobiology 43(6):387–99.Google Scholar
O'Keefe, J. & Dostrovsky, J. (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research 34(1):171–75.Google Scholar
O'Keefe, J. & Nadel, L. (1978) The hippocampus as a cognitive map. Clarendon Press.Google Scholar
Oman, C. (2007) Spatial orientation and navigation in microgravity. In: Spatial processing in navigation, imagery and perception, ed. Mast, F. W. & Jancke, L.. Springer.Google Scholar
Oman, C. M., Lichtenberg, B. K., Money, K. E. & McCoy, R. K. (1986) M.I.T./Canadian vestibular experiments on the Spacelab-1 mission: 4. Space motion sickness: Symptoms, stimuli, and predictability. Experimental Brain Research 64(2):316–34.Google Scholar
Phillips, F. & Layton, O. (2009) The traveling salesman problem in the natural environment. Journal of Vision 9(8):1145.Google Scholar
Pick, H. L. & Rieser, J. J. (1982) Children's cognitive mapping. In: Spatial orientation: Development and physiological bases, ed. Potegal, M., pp. 107–28. Academic Press.Google Scholar
Proffitt, D. R., Bhalla, M., Gossweiler, R. & Midgett, J. (1995) Perceiving geographical slant. Psychonomic Bulletin and Review 2(4):409–28.Google Scholar
Restat, J. D., Steck, S. D., Mochnatzki, H. F. & Mallot, H. A. (2004) Geographical slant facilitates navigation and orientation in virtual environments. Perception 33(6):667–87.Google Scholar
Riener, C. R., Stefanucci, J. K., Proffitt, D. R. & Clore, G. (2011) An effect of mood on the perception of geographical slant. Cognition and Emotion 25(1):174–82.Google Scholar
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B. L., Witter, M. P., Moser, M. B. & Moser, E. I. (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312(5774):758–62.Google Scholar
Schäfer, M. & Wehner, R. (1993) Loading does not affect measurement of walking distance in desert ants Cataglyphis fortis . Verhandlungen der Deutschen Zoologischen Gesellschaft 86:270.Google Scholar
Schnall, S., Harber, K. D., Stefanucci, J. K. & Proffitt, D. R. (2012) Social support and the perception of geographical slant. Journal of Experimental Social Psychology 44:1246–55.Google Scholar
Seidl, T. & Wehner, R. (2008) Walking on inclines: How do desert ants monitor slope and step length. Frontiers in Zoology 5:8.Google Scholar
Shinder, M. E. & Taube, J. S. (2010) Responses of head direction cells in the anterodorsal thalamus during inversion. Society for Neuroscience Abstracts, No. 895.1/FFF6. [Society of Neuroscience Meeting Planner 2010, San Diego, CA, Program No. 895.1.] (Online).Google Scholar
Stackman, R. W. & Taube, J. S. (1998) Firing properties of rat lateral mammillary single units: Head direction, head pitch, and angular head velocity. Journal of Neuroscience 18(21):9020–37.Google Scholar
Stackman, R. W., Tullman, M. L. & Taube, J. S. (2000) Maintenance of rat head direction cell firing during locomotion in the vertical plane. Journal of Neurophysiology 83(1):393–405.Google Scholar
Steck, S. D., Mochnatzki, H. F. & Mallot, H. A. (2003) The role of geographical slant in virtual environment navigation. In: Spatial Cognition III: Routes and navigation, human memory and learning, spatial representation and spatial learning. Lecture Notes in Artificial Intelligence, No. 2685, ed. Freksa, C., Brauer, W., Habel, C., & Wender, K. F., pp. 62–76. Springer.Google Scholar
Stefanucci, J. K., Proffitt, D. R., Banton, T. & Epstein, W. (2005) Distances appear different on hills. Perception and Psychophysics 67(6):1052–60.Google Scholar
Stefanucci, J. K., Proffitt, D. R., Clore, G. L. & Parekh, N. (2008) Skating down a steeper slope: Fear influences the perception of geographical slant. Perception 37(2):321–23.Google Scholar
Tafforin, C. & Campan, R. (1994) Ethological experiments on human orientation behavior within a three-dimensional space – in microgravity. Advances in Space Research 14(8):415–18.Google Scholar
Taube, J. S., Wang, S. S., Kim, S. Y. & Frohardt, R. J. (2013) Updating of the spatial reference frame of head direction cells in response to locomotion in the vertical plane. Journal of Neurophysiology 109(3):873–88.Google Scholar
Taube, J. S. (2007) The head direction signal: Origins and sensory-motor integration. Annual Review of Neuroscience 30:181–207.Google Scholar
Taube, J. S. & Burton, H. L. (1995) Head direction cell activity monitored in a novel environment and during a cue conflict situation. Journal of Neurophysiology 74(5):1953–71.Google Scholar
Taube, J. S., Muller, R. U. & Ranck, J. B. (1990a) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. Journal of Neuroscience 10(2):420–35.Google Scholar
Taube, J. S., Muller, R. U. & Ranck, J. B. (1990b) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. Journal of Neuroscience 10(2):436–47.Google Scholar
Taube, J. S., Stackman, R. W., Calton, J. L. & Oman, C. M. (2004) Rat head direction cell responses in zero-gravity parabolic flight. Journal of Neurophysiology 92(5):2887–997.Google Scholar
Tlauka, M., Wilson, P. N., Adams, M., Souter, C. & Young, A. H. (2007) An investigation into vertical bias effects. Spatial Cognition and Computation 7(4):365–91.Google Scholar
Tsoar, A., Nathan, R., Bartan, Y., Vyssotski, A., Dell'Omo, G. & Ulanovsky, N. (2011) Large-scale navigational map in a mammal. Proceedings of the National Academy of Sciences USA 108(37):E718–24. doi: 10.1073/pnas.1107365108.Google Scholar
Ulanovsky, N. & Moss, C. F. (2007) Hippocampal cellular and network activity in freely moving echolocating bats. Nature Neuroscience 10(2):224–33.Google Scholar
Valerio, S., Clark, B. J., Chan, J. H., Frost, C. P., Harris, M. J. & Taube, J. S. (2010) Directional learning, but no spatial mapping by rats performing a navigational task in an inverted orientation. Neurobiology of Learning and Memory 93(4):495–505.Google Scholar
Vidal, M., Amorim, M. A. & Berthoz, A. (2004) Navigating in a virtual three-dimensional maze: How do egocentric and allocentric reference frames interact? Brain Research. Cognitive Brain Research 19(3):244–58.Google Scholar
Walls, M. L. & Layne, J. E. (2009) Fiddler crabs accurately measure two-dimensional distance over three-dimensional terrain. The Journal of Experimental Biology 212(Pt. 20):3236–40.Google Scholar
Wang, R. F. & Spelke, E. S. (2002) Human spatial representation: Insights from animals. Trends in Cognitive Sciences 6(9):376.Google Scholar
Webber, D. M., Aitken, J. P. & O'Dor, R. K. (2000) Costs of locomotion and vertic dynamics of cephalopods and fish. Physiological and Biochemical Zoology 73(6):651–62.Google Scholar
Wehner, R. (2003) Desert ant navigation: How miniature brains solve complex tasks. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 189:579–88.Google Scholar
Wilson, P., Foreman, N., Stanton, D. & Duffy, H. (2004) Memory for targets in a multilevel simulated environment: Evidence for vertical asymmetry in spatial memory. Memory and Cognition 32(2):283–97.Google Scholar
Wintergerst, S. & Ronacher, B. (2012) Discrimination of inclined path segments by the desert ant Cataglyphis fortis . Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 198(5):363–73.Google Scholar
Wohlgemuth, S., Ronacher, B. & Wehner, R. (2001) Ant odometry in the third dimension. Nature 411(6839):795–98.Google Scholar
Young, L. R., Oman, C. M., Watt, D. G., Money, K. E. & Lichtenberg, B. K. (1984) Spatial orientation in weightlessness and readaptation to earth's gravity. Science 225(4658):205–208.Google Scholar
Zugaro, M. B., Arleo, A., Berthoz, A. & Wiener, S. I. (2003) Rapid spatial reorientation and head direction cells. Journal of Neuroscience 23(8):3478–82.Google Scholar