Navigation outside of the box: What the lab can learn from the field and what the field can learn from the lab

Movement Ecology

Volumn 2, Issue 1, 2014, Pages

  Jacobs, Lucia F ^a   Menzel, Randolf ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Cognitive map; Geometry; Hippocampus; Landmark; Locomotion; Parallel map theory

Indexed keywords

EID: 85014857886     PISSN: None     EISSN: 20513933     Source Type: Journal    
DOI: 10.1186/2051-3933-2-3     Document Type: Review

References (126)

1. Wiener J, Shettleworth SJ, Bingman VP, Cheng K, Healy SD, Jacobs LF, Jeffery KJ, Mallot HA, Menzel R, Newcombe NS: Animal Navigation - A Synthesis. In Animal Thinking. Edited by: Menzel R, Fisher J. Cambridge: MIT Press; 2011:1-33.
2. Tolman E: Cognitive maps in rats and men. Psych Rev 1948, 55:189-208.
3. Kramer G: Experiments on bird orientation. Ibis 1952, 94:265-285.
4. Griffin D: Bird navigation. Biol Rev 1952, 27:359-390.
5. O'Keefe J, Nadel L: The Hippocampus as a Cognitive Map. Oxford: Oxford University Press; 1978.
6. Lever C, Burton S, Jeewajee A, O'Keefe J, Burgess N: Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci 2009, 29:9771-9777.
7. Moser EI, Kropff E, Moser M-B: Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 2008, 31:69-89.
8. Kraus BJ, Robinson RJ II, White JA, Eichenbaum H, Hasselmo ME: Hippocampal "time cells": time versus path integration. Neuron 2013, 78:1-12.
9. Pfeiffer BE, Foster DJ: Hippocampal place-cell sequences depict future paths to remembered goals. Nature 2013, 497:74-81.
10. Wilson MA, McNaughton BL: Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
11. Anikeeva P, Andalman AS, Witten I, Warden M, Goshen I, Grosenick L, Gunaydin LA, Frank LM, Deisseroth K: Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat Neurosci 2011, 15:163-170.
12. Burgess N, Maguire EA, O'Keefe J: The human hippocampus and spatial and episodic memory. Neuron 2002, 35:625-641.
13. Grieves RM, Dudchenko PA: Cognitive maps and spatial inference in animals: Rats fail to take a novel shortcut, but can take a previously experienced one. Learn Motiv 2013, 44:81-92.
14. Shettleworth SJ: Cognition, Evolution, and Behavior. 2nd edition. New York: Oxford University Press; 2009.
15. Leonard B, McNaughton B: Spatial Representation in the rat: conceptual, behavioral, and neurophysiological perspectives. In Neurobiology of Comparative Cognition. Edited by: Kesner RP, Olton DS. Hillsdale, NJ: Lawrence Erlbaum Associates, Publishers; 1990:363-422.
16. Holland RA: The role of visual landmarks in the avian familiar area map. J Exp Biol 2003, 206:1773-1778.
17. Cartwright B, Collett T: Landmark learning in bees. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 1983, 151:521-543.
18. Philippides A, Baddeley B, Cheng K, Graham P: How might ants use panoramic views for route navigation? J Exper Biol 2011, 214:445-451.
19. Collett M: How desert ants use a visual landmark for guidance along a habitual route. Proc Natl Acad Sci USA 2010, 107:11638-11643.
20. Cruse H, Wehner R: No need for a cognitive map: decentralized memory for insect navigation. PLoS Comput Biol 2011, 7:e1002009.
21. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B: Path integration and the neural basis of the "cognitive map". Nat Rev Neurosci 2006, 7:663-678.
22. Filannino C, Armstrong C, Guilford T, Gagliardo A: Individual strategies and release site features determine the extent of deviation in clock-shifted pigeons at familiar sites. Anim Cogn 2013, 17:33-43.
23. Armstrong C, Wilkinson H, Meade J, Biro D, Freeman R, Guilford T: Homing pigeons respond to time-compensated solar cues even in sight of the loft. PLoS ONE 2013, 8:e63130.
24. Wiltschko R, Wiltschko W: Clock-shift experiments with homing pigeons: a compromise between solar and magnetic information? Behav Ecol Sociobiol 2001, 49:393-400.
25. Schiffner I, Pavkovic T, Siegmund B, Wiltschko R: Strategies of young pigeons during "map" learning. J Navig 2011, 64:431-448.
26. Schiffner I, Wiltschko R: Development of the navigational system in homing pigeons: increase in complexity of the navigational map. J Exper Biol 2013, 216:2675-2681.
27. Wallraff HG: Avian Navigation: Pigeon Homing as a Paradigm. Berlin: Springer; 2005.
28. Bovet J: Strategies of homing behavior in the red squirrel, Tamiasciurus hudsonicus. Behav Ecol Sociobiol 1984, 16:81-88.
29. Wikelski M, Kays RW, Kasdin NJ, Thorup K, Smith JA, Swenson GW: Going wild: what a global small-animal tracking system could do for experimental biologists. J Exper Biol 2007, 210:181-186.
30. Wehner R, Menzel R: Do insects have cognitive maps? Annu Rev Neurosci 1990, 13:403-414.
31. Dyer FC: Bees acquire route-based memories but not cognitive maps in a familiar landscape. Anim Behav 1991, 41:239-246.
32. Menzel R, Greggers U, Smith A, Berger S, Brandt R, Brunke S, Bundrock G, Hülse S, Plümpe T, Schaupp F: Honey bees navigate according to a map-like spatial memory. Proc Natl Acad Sci USA 2005, 102:3040.
33. Menzel R, Kirbach A, Haass W-D, Fischer B, Fuchs J, Koblofsky M, Lehmann K, Reiter L, Meyer H, Nguyen H, Jones S, Norton P, Greggers U: A common frame of reference for learned and communicated vectors in honeybee navigation. Curr Biol 2011, 21:645-650.
34. Meade J, Biro D, Guilford T: Homing pigeons develop local route stereotypy. Proc R Soc B Biol 2005, 272:17-23.
35. Gagliardo A, Filannino C, Ioale P, Pecchia T, Wikelski M, Vallortigara G: Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs. J Exper Biol 2011, 214:593-598.
36. Biro D, Meade J, Guilford T: Familiar route loyalty implies visual pilotage in the homing pigeon. Proc Natl Acad Sci U S A 2004, 101:17440-17443.
37. Wiltschko R, Schiffner I, Siegmund B: Homing flights of pigeons over familiar terrain. Anim Behav 2007, 74:1229-1240.
38. Lipp H, Vyssotski A, Wolfer D, Renaudineau S, Savini M, Tröster G, Dell'Omo G: Pigeon homing along highways and exits. Curr Biol 2004, 14:1239-1249.
39. Gagliardo A, Ioalè P, Savini M, Dell'omo G, Bingman VP: Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study. Eur J Neurosci 2009, 29:2389-2400.
40. Gagliardo A, Ioalè P, Savini M, Lipp H-P, Dell'omo G: Finding home: the final step of the pigeons' homing process studied with a GPS data logger. J Exp Biol 2007, 210:1132-1138.
41. Thorup K, Bisson I, Bowlin M, Holland R, Wingfield J, Ramenofsky M, Wikelski M: Evidence for a navigational map stretching across the continental US in a migratory songbird. Proc Natl Acad Sci USA 2007, 104:18115.
42. Tsoar A, Nathan R, Bartan Y, Vyssotski A, Dell'Omo G, Ulanovsky N: Large-scale navigational map in a mammal. Proc Natl Acad Sci USA 2011, 108:1-7.
43. Bingman VP, Gagliardo A, Hough GE, Ioalè P, Kahn MC, Siegel JJ: The avian hippocampus, homing in pigeons and the memory representation of large-scale space. Integr Comp Biol 2005, 45:555-564.
44. Jacobs LF: The role of social selection in the evolution of Hippocampal specialization. In Cognitive Biology: Evolutionary and Developmental Perspectives on Mind. Edited by: Tommasi L, Peterson MA, Nadel L. Cambridge, MA: MIT Press; 2009.
45. Papi F: Animal Homing. London: Chapman & Hall; 1992.
46. Gagliardo A: Forty years of olfactory navigation in birds. J Exper Biol 2013, 216:2165-2171.
47. Bingman VP, Ioale P, Casini G, Bagnoli P: Unimpaired acquisition of spatial reference memory, but impaired homing performance in hippocampal-ablated pigeons. Behav Brain Res 1988, 27:179-187.
48. Bingman VP: The importance of comparative studies and ecological validity for understanding hippocampal structure and cognitive function. Hippocampus 1992, 2:213-219.
49. Siegel JJ, Nitz D, Bingman VP: Lateralized functional components of spatial cognition in the avian hippocampal formation: evidence from single-unit recordings in freely moving homing pigeons. Hippocampus 2006, 16:125-140.
50. Bingman VP, Ioal P, Casini G, Bagnoli P: Hippocampal ablated homing pigeons show a persistent impairment in the time taken to return home. J Comp Physiol A 1988, 163:559-563.
51. Eichenbaum H, Stewart C, Morris RG: Hippocampal representation in place learning. J Neurosci 1990, 10:3531-3542.
52. Jacobs LF, Schenk F: Unpacking the cognitive map: the parallel map theory of hippocampal function. Psych Rev 2003, 110:285-315.
53. Kamil AC, Cheng K: Way-finding and landmarks: the multiple-bearings hypothesis. J Exp Biol 2001, 204:103-113.
54. Barkley C, Jacobs LF: Visual environment and delay affect cache retrieval accuracy in a food-storing rodent. Learn Behav 1998, 26:439-447.
55. Jacobs LF: From movement to transitivity: the role of hippocampal parallel maps in configural learning. Rev Neurosci 2006, 17:99-109.
56. Jacobs LF: The evolution of the cognitive map. Brain Behav Evol 2003, 62:128-139.
57. Kemp A, Manahan-Vaughan D: The Hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long-term depression. Cereb Cortex 2007, 18:968-977.
58. Hagena H, Manahan-Vaughan D: Learning-facilitated synaptic plasticity at CA3 mossy fiber and commissural-associational synapses reveals different roles in information processing. Cereb Cortex 2011, 21:2442-2449.
59. Striedter GF: Principles of Brain Evolution. Sunderland, MA: Sinauer Associates; 2005.
60. Jarvis ED: Evolution of the pallium in birds and reptiles. In Encyclopedia of Neuroscience. Edited by: Binder MD, Hirokawa N, Windhorst U. Berlin: Springer; 2009:1390-1400.
61. Hoogland PV, Vermeulen-Vanderzee E: Medial cortex of the lizard (gekko gecko): a hodological study with emphasis on regional specialization. J Comp Neurol 1993, 331:326-338.
62. Kahn MC, Hough GE, Eyck Ten GR, Bingman VP: Internal connectivity of the homing pigeon (Columba livia) Hippocampal formation: an anterograde and retrograde tracer study. J Comp Neurol 2003, 459:127-141.
63. Atoji Y, Wild JM: Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions. J Comp Neurol 2004, 475:426-461.
64. Székely AD: The avian hippocampal formation: subdivisions and connectivity. Behav Brain Res 1999, 98:219-225.
65. Gupta S, Maurya R, Saxena M, Sen J: Defining structural homology between the mammalian and avian hippocampus through conserved gene expression patterns observed in the chick embryo. Devel Biol 2012, 366:125-141.
66. Patzke N, Manns M, Güntürkün O, Ioalè P, Gagliardo A: Navigation-induced ZENK expression in the olfactory system of pigeons (Columba livia). Eur J Neurosci 2010, 31:2062-2072.
67. Kesner RP, Warthen DK: Implications of CA3 NMDA and opiate receptors for spatial pattern completion in rats. Hippocampus 2010, 20:550-557.
68. Salas C, Broglio C, Rodríguez F: Evolution of forebrain and spatial cognition in vertebrates: conservation across diversity. Brain Behav Evol 2003, 62:72-82.
69. Olton DS, Becker JT, Handelmann GE: Hippocampus, space and memory. Behav Brain Sci 1979, 2:352-365.
70. Bingman VP, Yates G: Hippocampal lesions impair navigational learning in experienced homing pigeons. Behav Neurosci 1992, 106:229-232.
71. Bingman VP, Ioale P, Casini G, Bagnoli P: The avian hippocampus: evidence for a role in the development of the homing pigeon navigational map. Behav Neurosci 1990, 104:906-911.
72. Bettis TJ, Jacobs LF: Sex differences in memory for landmark arrays in C57BL/J6 mice. Anim Cogn 2013, 16:873-882.
73. Rose E, Nagel P, Haag-Wackernagel D: Spatio-temporal use of the urban habitat by feral pigeons (Columba livia). Behav Ecol Sociobiol 2006, 60:242-254.
74. Jacobs LF: The ecology of spatial cognition: adaptive patterns of Hippocampal size and space use in wild Rodents. In Behavioural Brain Research in Naturalistic and Semi-Naturalistic Setting. Edited by: Alleva E, Fasolo A, Lipp H-P, Nadel L. Dordrecht: Springer; 1995:301-322.
75. Jacobs LF: From chemotaxis to the cognitive map: the function of olfaction. Proc Natl Acad Sci USA 2012, 109:10693-10700.
76. Konefal S, Elliot M, Crespi B: The adaptive significance of adult neurogenesis: an integrative approach. Front Neuroanat 2013, 7:21.
77. Miklos GL: Molecules and cognition: the latterday lessons of levels, language, and lac. Evolutionary overview of brain structure and function in some vertebrates and invertebrates. J Neurobiol 1993, 24:842-890.
78. Homberg U, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B: Central neural coding of sky polarization in insects. Philos Trans R Soc B, Biol Sci 2011, 366:680-687.
79. Heisenberg M: Mushroom body memoir: from maps to models. Nat Rev Neurosci 2003, 4:266-275.
80. Davis RL: Traces of Drosophila memory. Neuron 2011, 70:8-19.
81. Peng Y, Xi W, Zhang W, Zhang K, Guo A: Experience improves feature extraction in Drosophila. J Neurosci 2007, 27:5139-5145.
82. Able K: The concepts and terminology of bird navigation. J Avian Biol 2001, 32:174-183.
83. Bennett A: Do animals have cognitive maps? J Exper Biol 1996, 199:219-224.
84. Benhamou S: No evidence for cognitive mapping in rats. Anim Behav 1996, 52:201-212.
85. Foo P, Warren WH, Duchon A, Tarr MJ: Do humans integrate routes into a cognitive map? Map- versus landmark-based navigation of novel shortcuts. J Exper Psychol Learn Mem Cogn 2005, 31:195-215.
86. Etienne AS, Maurer R, Berlie J, Reverdin B, Rowe T, Georgakopoulos J, Séguinot V: Navigation through vector addition. Nature 1998, 396:161-164.
87. Russell JC, Mcmorland AJC, Mackay JWB: Exploratory behaviour of colonizing rats in novel environments. Anim Behav 2009, 79:159-164.
88. Gittleman JL: Carnivore olfactory bulb size: allometry, phylogeny and ecology. J Zool 1991, 225:253-272.
89. Roberts WA, Cruz C, Tremblay J: Rats take correct novel routes and shortcuts in an enclosed maze. J Exper Psych Anim B 2007, 33:79-91.
90. Hazen NL, Lockman JJ, Pick HL Jr: The development of children's representations of large-scale environments. Child Develop 1978, 49:623-636.
91. Maier NR: The effect of cerebral destruction on reasoning and learning in rats. J Comp Neurol 1932, 54:45-75.
92. Ellen P, Parko EM, Wages C, Doherty D, Herrmann T: Spatial problem solving by rats: Exploration and cognitive maps. Learn Motiv 1982, 13:81-94.
93. Ellen P, Soteres BJ, Wages C: Problem solving in the rat: piecemeal acquisition of cognitive maps. Anim Learn Behav 1984, 12:232-237.
94. Tolman E, Ritchie B, Kalish D: Studies in spatial learning: orientation and the short-cut. J Exper Psychol 1946, 36:13-24.
95. Gaulin SJ, FitzGerald RW: Sex differences in spatial ability: an evolutionary hypothesis and test. Am Nat 1986, 127:74-88.
96. Gaulin SJ, FitzGerald RW: Sexual selection for spatial-learning ability. Anim Behav 1989, 37:322-331.
97. Maier NR: A study of orientation in the rat. J Comp Psych 1932, 14:387.
98. Cheng K, Newcombe N: Is there a geometric module for spatial orientation? Squaring theory and evidence. Psych Bull Rev 2005, 12:1-23.
99. Tommasi L, Chiandetti C, Pecchia T, Sovrano VA, Vallortigara G: From natural geometry to spatial cognition. Neurosci Biobehav Rev 2012, 36:799-824.
100. Sovrano VA, Bisazza A, Vallortigara G: How fish do geometry in large and in small spaces. Anim Cogn 2006, 10:47-54.
101. Learmonth AE, Nadel L, Newcombe NS: Children's use of landmarks: implications for modularity theory. Psych Sci 2002, 13:337-341.
102. Sovrano VA, Vallortigara G: Dissecting the geometric module: a sense linkage for metric and landmark information in animals' spatial reorientation. Psych Sci 2006, 17:616-621.
103. Chiandetti C, Regolin L, Sovrano VA, Vallortigara G: Spatial reorientation: the effects of space size on the encoding of landmark and geometry information. Anim Cogn 2007, 10:159-168.
104. Chiandetti C, Vallortigara G: Spatial reorientation in large and small enclosures: comparative and developmental perspectives. Cogn Process 2008, 9:229-238.
105. Ulanovsky N: Neuroscience: how is three-dimensional space encoded in the brain? Curr Biol 2011, 21:R886-R888.
106. Yartsev MM, Witter MP, Ulanovsky N: Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 2011, 479:103-107.
107. Nardi D, Newcombe NS, Shipley TF: Reorienting with terrain slope and landmarks. Mem Cogn 2012, 41:214-228.
108. Nardi D, Newcombe NS, Shipley TF: The world is not flat: Can people reorient using slope? J Exper Psychol Learn Mem Cogn 2011, 37:354-367.
109. Nardi D, Nitsch KP, Bingman VP: Slope-driven goal location behavior in pigeons. J Exper Psych Anim B 2010, 36:430-442.
110. Menzel R, Fuchs J, Nadler L, Weiss B, Kumbischinski N, Adebiyi D, Hartfil S, Greggers U: Dominance of the odometer over serial landmark learning in honeybee navigation. Naturwissenschaften 2010, 97:763-767.
111. Collett TS: Rapid navigational learning in insects with a short lifespan. Connect Sci 1998, 10:255-270.
112. Boswell J, Womersley D: The Life of Samuel Johnson. London: Penguin Classics; 2008.
113. Waisman AS, Jacobs LF: Flexibility of cue use in the fox squirrel (Sciurus niger). Anim Cogn 2008, 11:625-636.
114. Visalberghi E, Limongelli L: Lack of comprehension of cause and effect relations in tool-using capuchin monkeys (Cebus apella). J Comp Psych 1994, 108:15-22.
115. Silva F, Silva K: Humans' folk physics is not enough to explain variations in their tool-using behavior. Psych Bull Rev 2006, 13:689-693.
116. Kolb B, Whishaw IQ: Brain plasticity and behavior. Annu Rev Psychol 1998, 49:43-64.
117. Fahrbach S, Moore D, Capaldi E, Farris S, Robinson G: Experience-expectant plasticity in the mushroom bodies of the honeybee. Learn Mem 1998, 5:115-123.
118. Durst C, Eichmüller S, Menzel R: Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav Neur Biol 1994, 62:259-263.
119. Gerstner JR, Yin JCP: Circadian rhythms and memory formation. Nat Neurosci 2010, 11:1-12.
120. Freake M, Muheim R, Phillips J: Magnetic maps in animals: a theory comes of age? Quart Rev Biol 2006, 81:327.
121. Wiltschko R, Wiltschko W: Magnetic Orientation in Animals. Berlin: Springer Verlag; 2012.
122. Lindauer M: Sonnenorientierung der Bienen under der Äquatorsonne und zur Nachtzeit. Naturwissenschaften 1957, 44:1-6.
123. Menzel R, Fischer J: Animal Thinking. Cambridge, MA: MIT Press; 2011.
124. Tommasi L, Peterson MA, Nadel L: Cognitive Biology: Evolutionary and Developmental Perspectives on Mind. Cambridge, MA: MIT Press; 2009.
125. Bingman VP, Bagnoli P, Ioal egrave P, Casini G: Homing behavior of pigeons after telencephalic ablations. Brain Behav Evol 1984, 24:94-108.
126. Einstein A: On the method of theoretical physics. Philosoph Sci 1934, 1:163-169.