Spatial cognition in bats and rats: From sensory acquisition to multiscale maps and navigation

Nature Reviews Neuroscience

Volumn 16, Issue 2, 2015, Pages 94-108

  Geva Sagiv, Maya ^a,b   Las, Liora ^a   Yovel, Yossi ^c   Ulanovsky, Nachum ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BAT; BRAIN MAPPING; COGNITION; NEURONAVIGATION; NONHUMAN; PERCEPTION; PRIORITY JOURNAL; REVIEW; SENSORY EVALUATION; SENSORY STIMULATION; SENSORY SYSTEM; SPATIAL ORIENTATION; THEORETICAL MODEL; ANIMAL; BIOLOGICAL MODEL; BRAIN; DEPTH PERCEPTION; PHYSIOLOGY; RAT;

RATTUS;

ANIMALS; BRAIN; CHIROPTERA; MODELS, NEUROLOGICAL; RATS; SPACE PERCEPTION; SPATIAL NAVIGATION;

EID: 84926484677     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3888     Document Type: Review

References (191)

1. Cochran, W. W., Mouritsen, H. & Wikelski, M. Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304, 405-408 (2004).
2. Wallraff, H. G. Avian Navigation: Pigeon Homing as a Paradigm (Springer, 2005).
3. Thorup, K. et al. Evidence for a navigational map stretching across the continental U.S. in a migratory songbird. Proc. Natl Acad. Sci. USA 104, 18115-18119 (2007).
4. Boles, L. C. & Lohmann, K. J. True navigation and magnetic maps in spiny lobsters. Nature 421, 60-63 (2003).
5. Muller, M. & Wehner, R. Path integration in desert ants, Cataglyphis fortis. Proc. Natl Acad. Sci. USA 85, 5287-5290 (1988).
6. Wittlinger, M., Wehner, R. & Wolf, H. The ant odometer: stepping on stilts and stumps. Science 312, 1965-1967 (2006).
7. Cheng, K., Narendra, A., Sommer, S. & Wehner, R. Traveling in clutter: navigation in the Central Australian desert ant Melophorus bagoti. Behav. Process. 80, 261-268 (2009).
8. Menzel, R. et al. Honey bees navigate according to a map-like spatial memory. Proc. Natl Acad. Sci. USA 102, 3040-3045 (2005).
9. Lohmann, K. J., Lohmann, C. M., Ehrhart, L. M., Bagley, D. A. & Swing, T. Animal behaviour: geomagnetic map used in sea-turtle navigation. Nature 428, 909-910 (2004).
10. Wu, L. Q. & Dickman, J. D. Neural correlates of a magnetic sense. Science 336, 1054-1057 (2012).
11. Zapka, M. et al. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274-1277 (2009).
12. Gagliardo, A., Ioale, P., Savini, M., Dell'Omo, G. &Bingman, V. P. Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study. Eur. J. Neurosci. 29, 2389-2400 (2009).
13. Kramer, G. Die sonnenorientierung der vögel. Verh. Dtsch. Zool. Ges. 1, 77-84 (1953).
14. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, 1978).
15. Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058 (1993).
16. O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425-428 (1996).
17. Hollup, S. A., Molden, S., Donnett, J. G., Moser, M.-B. & Moser, E. I. Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J. Neurosci. 21, 1635-1644 (2001).
18. Lee, I., Yoganarasimha, D., Rao, G. & Knierim, J. J. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430, 456-459 (2004).
19. Kjelstrup, K. B. et al. Finite scale of spatial representation in the hippocampus. Science 321, 140-143 (2008).
20. Harvey, C. D., Collman, F., Dombeck, D. A. &Tank, D. W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-946 (2009).
21. Royer, S., Sirota, A., Patel, J. & Buzsáki, G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 30, 1777-1787 (2010).
22. Epsztein, J., Lee, A. K., Chorev, E. & Brecht, M. Impact of spikelets on hippocampal CA1 pyramidal cell activity during spatial exploration. Science 327, 474-477 (2010).
23. Ulanovsky, N. & Moss, C. F. Hippocampal cellular and network activity in freely moving echolocating bats. Nature Neurosci. 10, 224-233 (2007).
24. Hafting, T., Fyhn, M., Molden, S., Moser, M.-B. &Moser, E. I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806 (2005).
25. Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758-762 (2006).
26. Barry, C., Hayman, R., Burgess, N. & Jeffery, K. J. Experience-dependent rescaling of entorhinal grids. Nature Neurosci. 10, 682-684 (2007).
27. Savelli, F., Yoganarasimha, D. & Knierim, J. J. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270-1282 (2008).
28. Boccara, C. N. et al. Grid cells in pre- and parasubiculum. Nature Neurosci. 13, 987-994 (2010).
29. Brandon, M. P. et al. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332, 595-599 (2011).
30. Yartsev, M. M., Witter, M. P. & Ulanovsky, N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103-107 (2011).
31. Taube, J. S., Muller, R. U. & Ranck, J. B. Jr. Headdirection cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420-435 (1990).
32. Zugaro, M. B., Tabuchi, E., Fouquier, C., Berthoz, A. & Wiener, S. I. Active locomotion increases peak firing rates of anterodorsal thalamic head direction cells. J. Neurophysiol. 86, 692-702 (2001).
33. Yoganarasimha, D., Yu, X. & Knierim, J. J. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J. Neurosci. 26, 622-631 (2006).
34. Taube, J. S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181-207 (2007).
35. Ulanovsky, N. & Moss, C. F. What the bat's voice tells the bat's brain. Proc. Natl Acad. Sci. USA 105, 8491-8498 (2008).
36. Villa, B. R. & Cockrum, E. L. Migration in the guano bat Tadarida brasiliensis mexicana (Saussure). J. Mammal. 43, 43-64 (1962).
37. Glass, B. P. Seasonal movements of Mexican freetail bats Tadarida brasiliensis mexicana banded in the Great Plains. Southwest. Nat. 27, 127-133 (1982).
38. Hutterer, R., Ivanova, T., Meyer-Cords, C. &Rodrigues, L. Bat Migrations in Europe: a Review of Banding Data and Literature (German Agency for Nature Conservation, 2005).
39. Richter, H. V. & Cumming, G. S. First application of satellite telemetry to track African straw-coloured fruit bat migration. J. Zool. 275, 172-176 (2008).
40. Winter, Y. & Stich, K. P. Foraging in a complex naturalistic environment: capacity of spatial working memory in flower bats. J. Exp. Biol. 208, 539-548 (2005).
41. Neuweiler, G. & Möhres, F. P. Die rolle des ortsgedachtnisses bei der orientierung der Grossblatt- Fledermaus, Megaderma Lyra. Zeit. Ver. Physiol. 57, 147-171 (1967).
42. Fiete, I. R., Burak, Y. & Brookings, T. What grid cells convey about rat location. J. Neurosci. 28, 6858-6871 (2008).
43. Sreenivasan, S. & Fiete, I. Grid cells generate an analog error-correcting code for singularly precise neural computation. Nature Neurosci. 14, 1330-1337 (2011).
44. Mathis, A., Herz, A. V. & Stemmler, M. B. Resolution of nested neuronal representations can be exponential in the number of neurons. Phys. Rev. Lett. 109, 018103 (2012).
45. Mathis, A., Herz, A. V. & Stemmler, M. Optimal population codes for space: grid cells outperform place cells. Neural Comput. 24, 2280-2317 (2012).
46. Hedrick, K. R. & Zhang, K. Megamap: continuous attractor model for place cells representing large environments (Poster). Program No. 578.01, Soc. Neurosci. Annual Meeting. San Diego (2013).
47. Ahissar, E. & Arieli, A. Figuring space by time. Neuron 32, 185-201 (2001).
48. Kepecs, A., Uchida, N. & Mainen, Z. F. The sniff as a unit of olfactory processing. Chem. Senses 31, 167-179 (2006).
49. Smear, M., Shusterman, R., O'Connor, R., Bozza, T. &Rinberg, D. Perception of sniff phase in mouse olfaction. Nature 479, 397-400 (2011).
50. Porter, J. et al. Mechanisms of scent-tracking in humans. Nature Neurosci. 10, 27-29 (2007).
51. Diamond, M. E., von Heimendahl, M., Knutsen, P. M., Kleinfeld, D. & Ahissar, E. 'Where' and 'what' in the whisker sensorimotor system. Nature Rev. Neurosci. 9, 601-612 (2008).
52. Griffin, D. R. Listening in the Dark (Yale Univ. Press, 1958). A seminal book in the field of animal behaviour, which described the discovery of bat echolocation and launched the field of animal biosonar.
53. Schnitzler, H.-U., Moss, C. F. & Denzinger, A. From spatial orientation to food acquisition in echolocating bats. Trends Ecol. Evolut. 18, 386-394 (2003).
54. Masters, W. M., Moffat, A. J. & Simmons, J. A. Sonar tracking of horizontally moving targets by the big brown bat Eptesicus fuscus. Science 228, 1331-1333 (1985).
55. Ghose, K. & Moss, C. F. Steering by hearing: a bat's acoustic gaze is linked to its flight motor output by a delayed, adaptive linear law. J. Neurosci. 26, 1704-1710 (2006).
56. Yovel, Y., Falk, B., Moss, C. F. & Ulanovsky, N. Optimal localization by pointing off axis. Science 327, 701-704 (2010).
57. Simmons, J. A. The resolution of target range by echolocating bats. J. Acoust. Soc. Am. 54, 157-173 (1973).
58. Simmons, J. A. Perception of echo phase information in bat sonar. Science 204, 1336-1338 (1979).
59. Riquimaroux, H., Gaioni, S. J. & Suga, N. Cortical computational maps control auditory perception. Science 251, 565-568 (1991).
60. Bell, G. P. & Fenton, M. B. The use of Doppler-shifted echoes as a flutter detection and clutter rejection system - the echolocation and feeding-behavior of Hipposideros ruber (Chiroptera, Hipposideridae). Behav. Ecol. Sociobiol.15, 109-114 (1984).
61. Schnitzler, H.-U. & Denzinger, A. Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals. J. Comp. Physiol. A 197, 541-559 (2011).
62. Simmons, J. A. et al. Target structure and echo spectral discrimination by echolocating bats. Science 186, 1130-1132 (1974).
63. Grunwald, J. E., Schörnich, S. & Wiegrebe, L. Classification of natural textures in echolocation. Proc. Natl Acad. Sci. USA 101, 5670-5674 (2004).
64. Simon, R., Holderied, M. W., Koch, C. U. & von Helversen, O. Floral acoustics: conspicuous echoes of a dish-shaped leaf attract bat pollinators. Science 333, 631-633 (2011).
65. Falk, B., Williams, T., Aytekin, M. & Moss, C. F. Adaptive behavior for texture discrimination by the free-flying big brown bat, Eptesicus fuscus. J. Comp. Physiol. A 197, 491-503 (2011).
66. Genzel, D. & Wiegrebe, L. Size does not matter: size-invariant echo-acoustic object classification. J. Comp. Physiol. A 199, 159-168 (2013).
67. Simmons, J. A., Fenton, M. B. & O'Farrell, M. J. Echolocation and pursuit of prey by bats. Science 203, 16-21 (1979).
68. Melcón, M. L., Denzinger, A. & Schnitzler, H.-U. Aerial hawking and landing: approach behaviour in Natterer's bats, Myotis nattereri (Kuhl 1818). J. Exp. Biol. 210, 4457-4464 (2007).
69. Skolnik, M. I. Introduction to Radar Systems (McGraw-Hill, 2001).
70. Berg, R. W. & Kleinfeld, D. Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J. Neurophysiol. 89, 104-117 (2003).
71. Mitchinson, B., Martin, C. J., Grant, R. A. &Prescott, T. J. Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc. Biol. Sci. 274, 1035-1041 (2007).
72. Grant, R. A., Mitchinson, B., Fox, C. W. &Prescott, T. J. Active touch sensing in the rat: anticipatory and regulatory control of whisker movements during surface exploration. J. Neurophysiol. 101, 862-874 (2009).
73. Deutsch, D., Pietr, M., Knutsen, P. M., Ahissar, E. &Schneidman, E. Fast feedback in active sensing: touchinduced changes to whisker-object interaction. PLoS ONE 7, e44272 (2012).
74. McCamy, M. B., Otero-Millan, J., Di Stasi, L. L., Macknik, S. L. & Martinez-Conde, S. Highly informative natural scene regions increase microsaccade production during visual scanning. J. Neurosci. 34, 2956-2966 (2014).
75. Jakobsen, L. & Surlykke, A. Vespertilionid bats control the width of their biosonar sound beam dynamically during prey pursuit. Proc. Natl Acad. Sci. USA 107, 13930-13935 (2010).
76. Yovel, Y., Falk, B., Moss, C. F. & Ulanovsky, N. Active control of acoustic field-of-view in a biosonar system. PLoS Biol. 9, e1001150 (2011).
77. Lawrence, B. D. & Simmons, J. A. Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. J. Acoust. Soc. Am. 71, 585-590 (1982).
78. Holderied, M. W. & von Helversen, O. Echolocation range and wingbeat period match in aerial-hawking bats. Proc. Biol. Sci. 270, 2293-2299 (2003).
79. Boonman, A., Bar-On, Y., Cvikel, N. & Yovel, Y. It's not black or white - on the range of vision and echolocation in echolocating bats. Front. Physiol. 4, 248 (2013).
80. Stilz, W. P. & Schnitzler, H.-U. Estimation of the acoustic range of bat echolocation for extended targets. J. Acoust. Soc. Am. 132, 1765-1775 (2012).
81. Williams, T. C., Williams, J. M. & Griffin, D. R. The homing ability of the neotropical bat Phyllostomus hastatus, with evidence for visual orientation. Anim. Behav. 14, 468-473 (1966).
82. Tsoar, A. et al. Large-scale navigational map in a mammal. Proc. Natl Acad. Sci. USA 108, E718-724 (2011).
83. Neuweiler, G. The Biology of Bats (Oxford Univ. Press, 2000).
84. Heffner, R. S., Koay, G. & Heffner, H. E. Sound localization in an Old-World fruit bat (Rousettus aegyptiacus): acuity, use of binaural cues, and relationship to vision. J. Comp. Psychol. 113, 297-306 (1999).
85. Childs, S. B. & Buchler, E. R. Perception of simulated stars by Eptesicus fuscus (Vespertilionidae): A potential navigational mechanism. Anim. Behav. 29, 1028-1035 (1981).
86. Jacobs, L. F. From chemotaxis to the cognitive map: the function of olfaction. Proc. Natl Acad. Sci. USA 109, 10693-10700 (2012).
87. Sterbing-D'Angelo, S. et al. Bat wing sensors support flight control. Proc. Natl Acad. Sci. USA 108, 11291-11296 (2011).
88. Horowitz, S. S., Cheney, C. A. & Simmons, J. A. Interaction of vestibular, echolocation, and visual modalities guiding flight by the big brown bat, Eptesicus fuscus. J. Vestib. Res. 14, 17-32 (2004).
89. Holland, R. A., Thorup, K., Vonhof, M. J., Cochran, W. W. & Wikelski, M. Navigation: bat orientation using Earth's magnetic field. Nature 444, 702 (2006).
90. Wang, Y., Pan, Y., Parsons, S., Walker, M. & Zhang, S. Bats respond to polarity of a magnetic field. Proc. Biol. Sci. 274, 2901-2905 (2007).
91. Holland, R. A., Borissov, I. & Siemers, B. M. A nocturnal mammal, the greater mouse-eared bat, calibrates a magnetic compass by the sun. Proc. Natl Acad. Sci. USA 107, 6941-6945 (2010).
92. Laska, M. Olfactory Sensitivity to food odor components in the short-tailed fruit bat, Carollia perspicillata (Phyllostomatidae, Chiroptera). J. Comp. Physiol. A 166, 395-399 (1990).
93. Stackman, R. W. & Taube, J. S. Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J. Neurosci. 17, 4349-4358 (1997).
94. O'Keefe, J. in The Hippocampus Book (eds Andersen, P., Morris, R. G., Amaral, D. G., Bliss, T. V. & O'Keefe, J.) 475-549 (Oxford Univ. Press, 2007).
95. Moser, E. I., Kropff, E. & Moser, M.-B. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69-89 (2008).
96. 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).
97. Pfeiffer, B. E. & Foster, D. J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74-79 (2013).
98. O'Keefe, J. & Conway, D. H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 31, 573-590 (1978).
99. Muller, R. U. & Kubie, J. L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951-1968 (1987).
100. Derdikman, D. & Moser, E. I. A manifold of spatial maps in the brain. Trends Cogn. Sci. 14, 561-569 (2010).
101. Solstad, T., Moser, E. I. & Einevoll, G. T. From grid cells to place cells: a mathematical model. Hippocampus 16, 1026-1031 (2006).
102. McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I. & Moser, M.-B. Path integration and the neural basis of the 'cognitive map'. Nature Rev. Neurosci. 7, 663-678 (2006).
103. Solstad, T., Boccara, C. N., Kropff, E., Moser, M.-B. &Moser, E. I. Representation of geometric borders in the entorhinal cortex. Science 322, 1865-1868 (2008).
104. Lever, C., Burton, S., Jeewajee, A., O'Keefe, J. &Burgess, N. Boundary vector cells in the subiculum of the hippocampal formation. J. Neurosci. 29, 9771-9777 (2009).
105. Taube, J. S. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15, 70-86 (1995).
106. Knierim, J. J., Kudrimoti, H. S. & McNaughton, B. L. Place cells, head direction cells, and the learning of landmark stability. J. Neurosci. 15, 1648-1659 (1995).
107. Rubin, A., Yartsev, M. M. & Ulanovsky, N. Encoding of head direction by hippocampal place cells in bats. J. Neurosci. 34, 1067-1080 (2014).
108. Tolman, E. C. Cognitive maps in rats and men. Psychol. Rev. 55, 189-208 (1948).
109. McHugh, T. J., Blum, K. I., Tsien, J. Z., Tonegawa, S. &Wilson, M. A. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87, 1339-1349 (1996).
110. Ono, T., Nakamura, K., Nishijo, H. & Eifuku, S. Monkey hippocampal neurons related to spatial and nonspatial functions. J. Neurophysiol. 70, 1516-1529 (1993).
111. Ekstrom, A. D. et al. Cellular networks underlying human spatial navigation. Nature 425, 184-188 (2003).
112. Killian, N. J., Jutras, M. J. & Buffalo, E. A. A map of visual space in the primate entorhinal cortex. Nature 491, 761-764 (2012).
113. Jacobs, J. et al. Direct recordings of grid-like neuronal activity in human spatial navigation. Nature Neurosci. 16, 1188-1190 (2013).
114. Las, L. & Ulanovsky, N. in Space, Time and Memory in the Hippocampal Formation (eds Derdikman, D. &Knierim, J. J.) 431-465 (Springer, 2014).
115. Etienne, A. S. & Jeffery, K. J. Path integration in mammals. Hippocampus 14, 180-192 (2004).
116. Etienne, A. S. et al. Navigation through vector addition. Nature 396, 161-164 (1998).
117. Cheung, A., Zhang, S., Stricker, C. & Srinivasan, M. V. Animal navigation: the difficulty of moving in a straight line. Biol. Cybern. 97, 47-61 (2007).
118. Cheung, A. Animal path integration: a model of positional uncertainty along tortuous paths. J. Theor. Biol. 341, 17-33 (2014).
119. Hartley, T., Burgess, N., Lever, C., Cacucci, F. &O'Keefe, J. Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10, 369-379 (2000).
120. Barry, C. et al. The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 17, 71-97 (2006).
121. Taylor, K. D. Range of movement and activity of common rats (Rattus norvegicus) on agricultural land. J. Appl. Ecol. 15, 663-677 (1978).
122. Strosslin, T., Sheynikhovich, D., Chavarriaga, R. &Gerstner, W. Robust self-localisation and navigation based on hippocampal place cells. Neural Netw. 18, 1125-1140 (2005).
123. Sheynikhovich, D., Chavarriaga, R., Strosslin, T., Arleo, A. & Gerstner, W. Is there a geometric module for spatial orientation? Insights from a rodent navigation model. Psychol. Rev. 116, 540-566 (2009).
124. Zeil, J. Visual homing: an insect perspective. Curr. Opin. Neurobiol. 22, 285-293 (2012).
125. Dupret, D., O'Neill, J., Pleydell-Bouverie, B. &Csicsvari, J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nature Neurosci. 13, 995-1002 (2010).
126. Jensen, M. E., Moss, C. F. & Surlykke, A. Echolocating bats can use acoustic landmarks for spatial orientation. J. Exp. Biol. 208, 4399-4410 (2005).
127. Zadicario, P., Avni, R., Zadicario, E. & Eilam, D. 'Looping' - an exploration mechanism in a dark open field. Behav. Brain Res. 159, 27-36 (2005).
128. Avni, R., Zadicario, P. & Eilam, D. Exploration in a dark open field: a shift from directional to positional progression and a proposed model of acquiring spatial information. Behav. Brain Res. 171, 313-323 (2006).
129. Mendelssohn, H. & Yom-Tov, Y. Fauna Palaestina: Mammalia of Israel (The Israel Academy of Sciences and Humanities, 1999).
130. Cnotka, J., Möhle, M. & Rehkämper, G. Navigational experience affects hippocampus size in homing pigeons. Brain Behav. Evol. 72, 233-238 (2008).
131. Jacobs, L. F., Gaulin, S. J., Sherry, D. F. &Hoffman, G. E. Evolution of spatial cognition: sexspecific patterns of spatial behavior predict hippocampal size. Proc. Natl Acad. Sci. USA 87, 6349-6352 (1990).
132. Safi, K. & Dechmann, D. K. Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera). Proc. Biol. Sci. 272, 179-186 (2005).
133. Maguire, E. A. et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl Acad. Sci. USA 97, 4398-4403 (2000).
134. Yartsev, M. M. & Ulanovsky, N. Representation of three-dimensional space in the hippocampus of flying bats. Science 340, 367-372 (2013).
135. Amaral, D. & Lavenex, P. in The Hippocampus Book (eds Andersen, P., Morris, R. G., Amaral, D. G., Bliss, T. V. & O'Keefe, J.) 37-115 (Oxford Univ. Press, 2007).
136. Fenton, A. A. et al. 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. J. Neurosci. 28, 11250-11262 (2008).
137. Park, E., Dvorak, D. & Fenton, A. A. Ensemble place codes in hippocampus: CA1, CA3, and dentate gyrus place cells have multiple place fields in large environments. PLoS ONE 6, e22349 (2011).
138. Jung, M. W., Wiener, S. I. & McNaughton, B. L. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14, 7347-7356 (1994).
139. Maurer, A. P., VanRhoads, S. R., Sutherland, G. R., Lipa, P. & McNaughton, B. L. Self-motion and the origin of differential spatial scaling along the septotemporal axis of the hippocampus. Hippocampus 15, 841-852 (2005).
140. Poucet, B., Thinus-Blanc, C. & Muller, R. U. Place cells in the ventral hippocampus of rats. Neuroreport 5, 2045-2048 (1994).
141. Brun, V. H. et al. Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18, 1200-1212 (2008).
142. Stensola, H. et al. The entorhinal grid map is discretized. Nature 492, 72-78 (2012).
143. Barry, C., Ginzberg, L. L., O'Keefe, J. & Burgess, N. Grid cell firing patterns signal environmental novelty by expansion. Proc. Natl Acad. Sci. USA 109, 17687-17692 (2012).
144. Worden, R. Navigation by fragment fitting: a theory of hippocampal function. Hippocampus 2, 165-187 (1992).
145. Wolbers, T. & Wiener, J. M. Challenges for identifying the neural mechanisms that support spatial navigation: the impact of spatial scale. Front. Hum. Neurosci. 8, 571 (2014).
146. Montello, D. R. in Spatial Information Theory: a Theoretical Basis for GIS, European Conference COSIT 1993, Lecture Notes in Computer Science 716 (eds Hirtle, S. C. & Frank, A. U.) 312-321 (Springer, 1993).
147. Meilinger, T. in Spatial Cognition VI: Learning, Reasoning, and Talking About Space, International Conference Spatial Cognition (eds Freksa, C., Newcombe, N.S., Gärdenfors, P. & Wölfl, S.) 344-360 (Springer, 2008).
148. Rich, P. D., Liaw, H. P. & Lee, A. K. Large environments reveal the statistical structure governing hippocampal representations. Science 345, 814-817 (2014).
149. Derdikman, D. et al. Fragmentation of grid cell maps in a multicompartment environment. Nature Neurosci. 12, 1325-1332 (2009).
150. Nitz, D. A. Tracking route progression in the posterior parietal cortex. Neuron 49, 747-756 (2006).
151. Whitlock, J. R., Pfuhl, G., Dagslott, N., Moser, M.-B. &Moser, E. I. Functional split between parietal and entorhinal cortices in the rat. Neuron 73, 789-802 (2012).
152. Harvey, C. D., Coen, P. & Tank, D. W. Choice-specific sequences in parietal cortex during a virtualnavigation decision task. Nature 484, 62-68 (2012).
153. Wilber, A. A., Clark, B. J., Forster, T. C., Tatsuno, M. & McNaughton, B. L. Interaction of egocentric and world-centered reference frames in the rat posterior parietal cortex. J. Neurosci. 34, 5431-5446 (2014).
154. Wood, E. R., Dudchenko, P. A., Robitsek, R. J. &Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623-633 (2000).
155. Johnson, A. & Redish, A. D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176-12189 (2007).
156. Whitlock, J. R., Sutherland, R. J., Witter, M. P., Moser, M. -B. & Moser, E. I. Navigating from hippocampus to parietal cortex. Proc. Natl Acad. Sci. USA 105, 14755-14762 (2008).
157. Foster, D. J. & Knierim, J. J. Sequence learning and the role of the hippocampus in rodent navigation. Curr. Opin. Neurobiol. 22, 294-300 (2012).
158. Smirnakis, S. M., Berry, M. J., Warland, D. K., Bialek, W. & Meister, M. Adaptation of retinal processing to image contrast and spatial scale. Nature 386, 69-73 (1997).
159. Fairhall, A. L., Lewen, G. D., Bialek, W. & de Ruyter Van Steveninck, R. R. Efficiency and ambiguity in an adaptive neural code. Nature 412, 787-792 (2001).
160. Ulanovsky, N., Las, L. & Nelken, I. Processing of lowprobability sounds by cortical neurons. Nature Neurosci. 6, 391-398 (2003).
161. Ulanovsky, N., Las, L., Farkas, D. & Nelken, I. Multiple time scales of adaptation in auditory cortex neurons. J. Neurosci. 24, 10440-10453 (2004).
162. Antunes, F. M., Nelken, I., Covey, E. &Malmierca, M. S. Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS ONE 5, e14071 (2010).
163. Burak, Y. & Fiete, I. R. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 5, e1000291 (2009).
164. Finkelstein, A. et al. Three-dimensional head-direction coding in the bat brain. Nature 517, 159-164 (2015).
165. Jones, G. & Holderied, M. W. Bat echolocation calls: adaptation and convergent evolution. Proc. Biol. Sci. 274, 905-912 (2007).
166. Gillam, E. H., Ulanovsky, N. & McCracken, G. F. Rapid jamming avoidance in biosonar. Proc. Biol. Sci. 274, 651-660 (2007).
167. Holderied, M. W., Jones, G. & von Helversen, O. Flight and echolocation behaviour of whiskered bats commuting along a hedgerow: range-dependent sonar signal design, Doppler tolerance and evidence for 'acoustic focussing'. J. Exp. Biol. 209, 1816-1826 (2006).
168. Jutras, M. J., Fries, P. & Buffalo, E. A. Oscillatory activity in the monkey hippocampus during visual exploration and memory formation. Proc. Natl Acad. Sci. USA 110, 13144-13149 (2013).
169. Peebles, P. Z. Radar Principles (Wiley, 1998).
170. Jones, G. Echolocation. Curr. Biol. 15, R484-R488 (2005).
171. Aikath, D., Weible, A. P., Rowland, D. C. &Kentros, C. G. Role of self-generated odor cues in contextual representation. Hippocampus (2014).
172. Zhang, S., Schönfeld, F., Wiskott, L. & Manahan- Vaughan, D. Spatial representations of place cells in darkness are supported by path integration and border information. Front. Behav. Neurosci. 8, 222 (2014).
173. Battaglia, F. P., Sutherland, G. R. & McNaughton, B. L. Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus. J. Neurosci. 24, 4541-4550 (2004).
174. Olypher, A. V., Lansky, P., Muller, R. U. & Fenton, A. A. Quantifying location-specific information in the discharge of rat hippocampal place cells. J. Neurosci. Methods 127, 123-135 (2003).
175. Ulanovsky, N. & Moss, C. F. Dynamics of hippocampal spatial representation in echolocating bats. Hippocampus 21, 150-161 (2011).
176. Yovel, Y., Geva-Sagiv, M. & Ulanovsky, N. Click-based echolocation in bats: not so primitive after all. J. Comp. Physiol. A 197, 515-530 (2011).
177. Gallistel, C. R. The Organization of Learning (MIT Press, 1990).
178. Buchler, E. R. & Childs, S. B. Orientation to distant sounds by foraging big brown bats (Eptesicus fuscus). Anim. Behav. 29, 428-432 (1981).
179. Blatcheley, W. S. in Indiana Caves and their Fauna. Indiana Department of Geology and Natural Resources, 21st Annual Report 121-212 (1896).
180. Mittelstaedt, M. L. & Mittelstaedt, H. in Avian Navigation (eds Papi, F. & Wallraff, H. G.) 290-297 (Springer, 1982).
181. Wolf, H. Odometry and insect navigation. J. Exp. Biol. 214, 1629-1641 (2011).
182. Wehner, R. & Wehner, S. Path Integration in desert ants - approaching a long-standing puzzle in insect navigation. Monit. Zool. Ital. 20, 309-331 (1986).
183. Maaswinkel, H. & Whishaw, I. Q. Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav. Brain Res. 99, 143-152 (1999).
184. Höller, P. & Schmidt, U. The orientation behaviour of the lesser spearnosed bat, Phyllostomus discolor (Chiroptera) in a model roost. J. Comp. Physiol. A 179, 245-254 (1996).
185. Höller, P. Orientation by the bat Phyllostomus discolor (Phyllostomidae) on the return flight to its roosting place. Ethology 100, 72-83 (1995).
186. Bennett, A. T. Do animals have cognitive maps? J. Exp. Biol. 199, 219-224 (1996).
187. Wiltschko, R. & Wiltschko, W. Magnetoreception. Adv. Exp. Med. Biol. 739, 126-141 (2012).
188. Riggs, L. A. in Vision and Visual Perception (ed. Graham, C. H.) 321-349 (Wiley, 1965).
189. Suthers, R. A. in Biology of Bats (ed. Wimsatt, W. A.) 265-309 (Academic Press, 1970).
190. Moulton, D. G. & Eayrs, J. T. Studies in olfactory acuity: II. Relative detectability of n-aliphatic alcohols by the rat. Q. J. Exp. Psychol. 12, 99-109 (1960).
191. Moulton, D. G. Studies in olfactory acuity: III. relative detectability of n-aliphatic acetates by the rat. Q. J. Exp. Psychol. 12, 203-213 (1960).