Path integration in mammals

Hippocampus

Volumn 14, Issue 2, 2004, Pages 180-192

  Etienne, Ariane S ^a   Jeffery, Kathryn J ^b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cognitive map; Hippocampus; Landmarks; Navigation; Path integration; Self motion cues

Indexed keywords

ANALYTICAL ERROR; ANIMAL BEHAVIOR; ASSOCIATION; BRAIN NERVE CELL; CALCULATION; CELL POPULATION; COGNITION; CORRELATION ANALYSIS; HUMAN; MAMMAL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SPATIAL DISCRIMINATION; SPATIAL MEMORY;

ANIMALS; CUES; HIPPOCAMPUS; HUMANS; MAMMALS; ORIENTATION; SPACE PERCEPTION;

EID: 1842679227     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.10173     Document Type: Review

References (131)

1. Alyan S, Jander R. 1994. Short-range homing in the house mouse, Mus musculus: stages in the learning of directions. Anim Behav 48:285-298.
2. Alyan S, McNaughton BL. 1999. Hippocampectomized rats are capable of homing by path integration. Behav Neurosci 113:19-31.
3. Arleo A, Gerstner W. 2000. Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity. Biol Cybern 83:287-299.
4. Bassett JP, Taube JS. 2001. Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J Neurosci 21:5740-5751.
5. Benhamou S. 1997. Path integration by swimming rats. Anim Behav 54:321-327.
6. Benhamou S, Sauvé JP, Bovet P. 1990. Spatial memory in large scale movements: efficiency and limitation of the egocentric coding process. J Theor Biol 145:1-12.
7. Berthoz A, Amorim M-A, Glasauer S, Grasso R, Takei Y, Viaud-Delmon I. 1999. Dissociation between distance and direction during locomotor navigation. In: Golledge RG, editor. Wayfinding behavior. Baltimore, MD: Johns Hopkins University Press. p 328-348.
8. Biegler R, Morris RG. 1993. Landmark stability is a prerequisite for spatial but not discrimination learning. Nature 361:631-633.
9. Bisetzky AR. 1957. Zeitschrift für vergleichende Physiologie: 40:264-288.
10. Blair HT, Lipscomb BW, Sharp PE. 1997. Anticipatory time intervals of head-direction cells in the anterior thalamus of the rat: implications for path integration in the head-direction circuit. J Neurophysiol 78:145-159.
11. Blair HT, Sharp PE. 1996. Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat. Behav Neurosci 110:643-660.
12. Burgess N, Jeffery KJ, O'Keefe J. 1998. Introduction. In: Burgess N, Jeffery KJ, O'Keefe J, editors. The hippocampal and parietal foundations of spatial cognition. Oxford: Oxford University Press. p 3-31.
13. Chen LL, Lin LH, Barnes CA, McNaughton BL. 1994. Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res 101: 24-34.
14. Cheng K, Spetch ML. 1998. Mechanisms of landmark use in mammals and birds. In: Healy S, editor. New York: Oxford University Press. p 1-17.
15. Cohen HS. 2000. Vestibular disorders and impaired path integration along a linear trajectory. J Vestib Res 10:7-15.
16. Collett M, Collett TS. 2000. How do insects use path integration for their navigation? Biol Cybern 83:245-259.
17. Cooper BG, Mizumori SJ. 1999. Retrosplenial cortex inactivation selectively impairs navigation in darkness. NeuroReport 10:625-630.
18. Cooper BG, Mizumori SJ. 2001. Temporary inactivation of the retrosplenial cortex causes a transient reorganization of spatial coding in the hippocampus. J Neurosci 21:3986-4001.
19. Darwin C. 1873. Origin of certain instincts. Nature 7:417-418.
20. Etienne AS. 1998. Mammalian navigation, neural models and biorobotics. Connection Sci 10:271-289.
21. Etienne AS. 2003. How does path integration interact with olfaction, vision and the representation of space? In: Jeffery KJ, editor. The neurobiology of spatial behaviour. Oxford: Oxford University Press (in press).
22. Etienne AS, Maurer R, Saucy F, Teroni E. 1986. Short-distance homing in the golden hamster after a passive outward journey. Anim Behav 34:696-715.
23. Etienne AS, Maurer R, Saucy F. 1988. Limitations in the assessment of path dependent information. Behavior 106:81-111.
24. Etienne AS, Teroni E, Portenier V, Hurni C. 1990. The effect of a single light cue on homing behaviour of the golden hamster. Anim Behav 39:17-41.
25. Etienne AS, Maurer R, Séguinot V. 1996. Path integration in mammals and its interaction with visual landmarks. J Exp Biol 199:201-209.
26. Etienne AS, Maurer R, Berlie J, Reverdin B, Rowe T, Georgakopoulos J, Séguinot V. 1998. Navigation through vector addition. Nature 396: 161-164.
27. Etienne AS, Boulens V, Maurer R, Rowe T, Siegrist C. 2000. A brief view of known landmarks reorientates path integration in hamsters. Naturwissenschaften 87:494-498.
28. Fujita N, Loomis JM, Klatzky RL, Golledge RG. 1990. A minimal representation for dead-reckoning navigation: updating the homing vector. Geogr Anal 22:326-335.
29. Gallistel CR. 1990. The organization of learning. Cambridge, MA: Bradford Books/MIT Press.
30. Gallistel CR, Cramer AE. 1996. Computations on metric maps in mammals: getting oriented and choosing a multi-destination route. J Exp Biol 199:211-217.
31. Glasauer S, Amorim MA, Viaud-Delmon I, Bethoz A. 1999. Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path. Exp Brain Res 135:489-497.
32. Glasauer S, Amorim MA, Vitte E, Berthoz A. 1994. Goal-directed linear locomotion in normal and labyrinthine-defective subjects. Exp Brain Res 98:323-335.
33. Goerner P. 1958. Die optische und kinästhetische Orientierung der Trichterspinne Agelena labyrinthica (CL.). Z Vergl Physiol 4 1:111-153.
34. Golani I, Benjamini Y, Eilam D. 1993. Stopping behavior: constraints on exploration in rats (Rattus norvegicus). Behav Brain Res 53:21-33.
35. Golob EJ, Taube JS. 1999. Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration. J Neurosci 19:7198-7211.
36. Goodridge JP, Taube JS. 1997. Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci 17:9315-9330.
37. Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS. 1998. Cue control and head direction cells. Behav Neurosci 112:749-761.
38. Gothard KM, Hoffman KL, Battaglia FP, McNaughton BL. 2001. Dentate gyrus and CA1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J Neurosci 21:7284-7292.
39. Gothard KM, Skaggs WE, McNaughton BL. 1996. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci 16:8027-8040.
40. Görner P, Möller P. 2001. Orientation and navigation in birds, humans and other animals. Proceedings of the 4th International Conference on Animal Navigation.
41. Guazzelli A, Bota M, Arbib MA. 2001. Competitive Hebbian learning and the hippocampal place cell system: modeling the interaction of visual and path integration cues. Hippocampus 11:216-239.
42. Harris LR, Jenkin M, Zikovitz DC. 2000. Visual and non-visual cues in the perception of linear self-motion. Exp Brain Res 135:12-21.
43. Hartmann G, Wehner R. 1995. The ant's path integration system: a neural architecture. Biol Cybern 73:483-497.
44. Hill AJ. 1978. First occurrence of hippocampal spatial firing in a new environment. Exp Neurol 62:282-297.
45. Hirase H, Czurko HH, Csicsvari J, Buzsaki G. 1999. Firing rate and theta-phase coding by hippocampal pyramidal neurons during "space clamping." Eur J Neurosci 11:4373-4380.
46. Israel I, Siegler I. 1999. Active reproduction of passive rotations and contingent eye movements. In: Current oculomotor research. New York: Plenum Press. p 133-136.
47. Israel I, Sievering D, Koenig E. 1995. Self-rotation estimate about the vertical axis. Acta Otolaryngol 115:3-8.
48. Israel I, Grasso R, Georges-Francois P, Tsuzuku T, Berthoz A. 1997. Spatial memory and path integration studied by self-driven passive linear displacement. I. Basic properties. J Neurophysiol 77:3180-3192.
49. Jander R. 1957. Die optische Richtungsorientiergun der roten Waldameise (Formica rufa L.). Z vergl Physiol 40:162-238.
50. Jeffery KJ. 1998. Learning of landmark stability and instability by hippocampal place cells. Neuropharmacology 37:677-687.
51. Jeffery KJ. 2000. Plasticity of the hippocampal cellular representation of place. In: Holscher C, editor. Neuronal mechanisms of memory formation. Cambridge: Cambridge University Press. p 100-121.
52. Jeffery KJ, Donnett JG, Burgess N, O'Keefe JM. 1997. Directional control of hippocampal place fields. Exp Brain Res 117:131-142.
53. Jeffery KJ, O'Keefe JM. 1999. Learned interaction of visual and idiothetic cues in the control of place field orientation. Exp Brain Res 127:151-161.
54. Kearns MJ, Warren WH, Duchon AP, Tarr MJ. 1902. Path integration from optic flow and body senses in a homing task. Perception 31:349-374.
55. Knierim JJ. 2002. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci 22:6254-6264.
56. Knierim JJ, Kudrimoti HS, McNaughton BL. 1995. Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15: 1648-1659.
57. Knierim JJ, Kudrimoti HS, McNaughton BL. 1996. Neuronal mechanisms underlying the interaction between visual landmarks and path integration in the rat. Int J Neural Syst 7:213-218.
58. Knierim JJ, Kudrimoti HS, McNaughton BL. 1998. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J Neurophysiol 80:425-446.
59. Landau B, Spelke E, Gleitman H. 1984. Spatial knowledge in a young blind child. Cognition 16:225-260.
60. Lever C, Wills T, Cacucci F, Burgess N, O'Keefe J. 2002. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416:90-94.
61. Lindauer M. 1963. Kompassorientierung. Ergebn Biol 26:158-181.
62. Loomis JM, Klatzky RL, Golledge RG, Cicinelli JG, Pellegrino JW, Fry PA. 1993. Nonvisual navigation by blind and sighted: assessment of path integration ability. J Exp Psychol Genet 122:73-91.
63. Loomis JM, Klatzky RL, GR, Philbeck JW. 1999. Human navigation by path integration. In: Golledge RG, editor. Wayfinding behavior. Baltimore, MD: Johns Hopkins University Press. p 125-151.
64. Maaswinkel H, Whishaw IQ. 1999. Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav Brain Res 99:143-152.
65. Maaswinkel H, Jarrard LE, Whishaw IQ. 1999. Hippocampectomized rats are impaired in homing by path integration. Hippocampus 9:553-561.
66. Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O'Keefe J. 1998. Knowing where and getting there: a human navigation network. Science 280:921-924.
67. Maurer R. 1998. A connectionist model of path integration with and without a representation of distance to the starting point. Psychobiology 26:21-35.
68. Maurer R, Séguinot V. 1995. What is modelling for? A critical review of the models of path integration. J Theor Biol 175:457-475.
69. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL. 1996. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199:173-185.
70. Merfeld DM, Zupan L, Peterka RJ. 1999. Humans use internal models to estimate gravity and linear acceleration. Nature 398:615-618.
71. Metcalfe T, Gresty M. 1992. Self-controlled reorienting movements in response to rotational displacements in normal subjects and patients with labyrinthine disease. Ann NY Acad Sci 656:695-698.
72. Mittelstaedt H. 1999. The role of the otoliths in perception of the vertical and in path integration. Ann N Y Acad Sci 871:334-344.
73. Mittelstaedt H. 2000. Triple-loop model of path control by head direction and place cells. Biol Cybern 83:261-270.
74. Mittelstaedt H, Mittelstaedt M-L. 1982. Homing by path integration. In: Papi F, Wallraff HG, editors. Avian navigation. New York: Springer. p 290-297.
75. Mittelstaedt ML, Mittelstaedt H. 2001. Idiothetic navigation in humans: estimation of path length. Exp Brain Res 139:318-332.
76. Mizumori SJ, Williams JD. 1993. Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015-4028.
77. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
78. Muller R. 1996. A quarter of a century of place cells. Neuron 17:813-822.
79. Muller RU, Kubie JL. 1987. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951-1968.
80. Müller M, Wehner R. 1988. Path integration in desert ants, Cataglyphis fortis. Proc Natl Acad Sci USA 85:5287-5290.
81. Müller M, Wehner R. 1994. The hidden spiral: systematic search and path integration in desert ants, Cataglyphis fortis. J Comp Physiol A 175: 525-530.
82. Murphy JJ. 1873. Instinct: a mechanical analogy. Nature 7:483.
83. Nadel L. 1999. Neural mechanisms of spatial orientation and wayfinding: an overview. In: Golledge RG, editor. Wayfinding behavior. Baltimore, MD: Johns Hopkins University Press. p 313-327.
84. O'Keefe J, Burgess N. 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381:425-428.
85. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
86. O'Keefe J, Nadel L. 1978. The hippocampus as a cognitive map. Oxford: Clarendon Press.
87. O'Keefe J, Speakman A. 1987. Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68:1-27.
88. O'Keefe J, Burgess N, Donnett JG, Jeffery KJ, Maguire EA. 1998. Place cells, navigational accuracy, and the human hippocampus. Philos Trans R Soc Lond B Biol Sci 353:1333-1340.
89. Quirk GJ, Muller RU, Kubie JL. 1990. The firing of hippocampal place cells in the dark depends on the rat's recent experience. J Neurosci 10:2008-2017.
90. Redish AD. 1999. Beyond the cognitive map. Cambridge, MA: The MIT Press.
91. Redish AD. 2001. The hippocampal debate: are we asking the right questions? Behav Brain Res 127:81-98.
92. Rieser J. 1999. Wayfinding behavior. In: Golledge RG, editor. Baltimore, MD: Johns Hopkins University Press. p 168-190.
93. Rotenberg A, Muller RU. 1997. Variable place-cell coupling to a continuously viewed stimulus: evidence that the hippocampus acts as a perceptual system. Philos Trans R Soc Lond B Biol Sci 352:1505-1513.
94. Samsonovich A, McNaughton BL. 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900-5920.
95. Save E, Cressant A, Thinus-Blanc C, Poucet B. 1998. Spatial firing of hippocampal place cells in blind rats. J Neurosci 18:1818-1826.
96. Save E, Nerad L, Poucet B. 2000. Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 10:64-76.
97. Save E, Guazzelli A, Poucet B. 2001. Dissociation of the effects of bilateral lesions of the dorsal hippocampus and parietal cortex on path integration in the rat. Behav Neurosci 115:1212-1223.
98. Séguinot V, Maurer R, Etienne AS. 1993. Dead reckoning in a small mammal: the evaluation of distance. J Comp Physiol A 173:103-113.
99. Séguinot V, Cattet J, Benhamou S. 1998. Path integration in dogs. Anim Behav 55:787-799.
100. Sharp PE, Blair HT, Etkin D, Tzanetos DB. 1995. Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. J Neurosci 15:173-189.
101. Sharp PE, Tinkelman A, Cho J. 2001. Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: implications for path integration in the head direction cell circuit. Behav Neurosci 115:571-588.
102. Siegrist C, Etienne AS, Boulens V, Maurer R, Rowe T. 2003. Homing by path integration in a new environment. Anim Behav 65:185-194.
103. Skaggs WE, McNaughton BL. 1998. Spatial firing properties of hippocampal CA1 populations in an environment containing two visually identical regions. J Neurosci 18:8455-8466.
104. Skaggs WE, Knierim JJ, Kudrimoti H, McNaughton BL. 1995. A model of the neural basis of the rat's sense of direction. In: Tesauro G, Touretzky DS, Leen TK, editors. Advances in neural information processing systems, Vol 7. Cambridge, MA: MIT Press. p 173-180.
105. Srinivasan MV, Zhang S, Altwein M, Tautz J. 2000. Honeybee navigation: nature and calibration of the "odometer." Science 287:851-853.
106. Stackman RW, Herbert AM. 2002. Rats with lesions of the vestibular system require a visual landmark for spatial navigation. Behav Brain Res 128:27-40.
107. Stringer SM, Trappenberg TP, Rolls ET, de Araujo I. 2002. Self-organizing continuous attractor networks and path integration: one-dimensional models of head direction cells. Network 13:217-242.
108. Tanila H, Shapiro ML, Eichenbaum H. 1997. Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7:613-623.
109. Taube JS. 1998. Head direction cells and the neurophysiological basis for a sense of direction. Prog Neurobiol 55:225-256.
110. Taube JS, Burton HL. 1995. Head direction cell activity monitored in a novel environment and during a cue conflict situation. J Neurophysiol 74:1953-1971.
111. Taube JS, Muller RU, Ranck-JB J. 1990. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10:436-447.
112. Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, Stackman RW. 1996. Processing the head direction cell signal: a review and commentary. Brain Res Bull 40:477-484.
113. Telford L, Howard IP, Ohmi M. 1995. Heading judgments during active and passive self-motion. Exp Brain Res 104:502-510.
114. van Groen T, Wyss JM. 1990. The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Res 529:165-177.
115. von Frisch K. 1967. The dance language and orientation of bees. Cambridge, MA: Harvard University Press.
116. Wallace DG, Hines DJ, Pellis SM, Whishaw IQ. 2002. Vestibular information is required for dead reckoning in the rat. J Neurosci 22:10009-10017.
117. Wang RF, Spelke ES. 2000. Updating egocentric representations in human navigation. Cognition 77:215-250.
118. Wehner R. 1994. The polarization-vision project: championing organismic biology. In: Schildberger K, Elsner N, editors. Neural basis of behavioural adaptation. New York: Gustav Fisher. p 103-143.
119. Wehner R, Menzel R. 1990. Do insects have cognitive maps? Annu Rev Neurosci 13:403-414.
120. Wehner R, Srinivasan MV. 1981. Searching behavior of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J Comp Physiol Psychol 142: 315-338.
121. Wehner R, Wehner S. 1990. Insect navigation: use of maps or Ariadne's thread? Ethol Ecol Evol 2:27-48.
122. Whishaw IQ, Gorny B. 1999. Path integration absent in scent-tracking fimbria-fornix rats: evidence for hippocampal involvement in "sense of direction" and "sense of distance" using self-movement cues. J Neurosci 19:4662-4673.
123. Whishaw IQ, Maaswinkel H. 1998. Rats with fimbria-fornix lesions are impaired in path integration: a role for the hippocampus in "sense of direction." J Neurosci 18:3050-3058.
124. Whishaw IQ, Cassel JC, Jarrard LE. 1995. Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J Neurosci 15:5779-5788.
125. Whishaw IQ, McKenna JE, Maaswinkel H. 1997. Hippocampal lesions and path integration. Curr Opin Neurobiol 7:228-234.
126. Wiener SI. 1993. Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13:3802-3817.
127. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058.
128. Wittman T, Schwegler H. 1995. Biol Cybern 73:569-579.
129. Wohlgemuth S, Ronacher B, Wehner R. 2001. Ant odometry in the third dimension. Nature 411:795-798.
130. Zhang K. 1996. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16:2112-2126.
131. Zill S, Seyfarth EA. 1996. Exoskeletal sensors for walking. Sci Am 275:70-74.