Representing the richness of avian spatial cognition: Properties of a lateralized homing pigeon hippocampus

Reviews in the Neurosciences

Volumn 17, Issue 1-2, 2006, Pages 17-28

  Bingman, Verner P ^a   Siegel, Jennifer J ^b   Gagliardo, Anna ^c   Erichsen, Jonathan T ^d  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PISA   (Italy)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Birds; Cognitive map; Hippocampal formation; Navigation; Spatial memory; Unit recording

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; BRAIN DAMAGE; BRAIN NERVE CELL; COGNITION; HEMISPHERIC DOMINANCE; HIPPOCAMPUS; LEARNING; NERVE POTENTIAL; NONHUMAN; PIGEON; PRIORITY JOURNAL; SPATIAL MEMORY; TASK PERFORMANCE;

EID: 33646387165     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/REVNEURO.2006.17.1-2.17     Document Type: Article

References (65)

1. Andrew RJ, Mench J, Rainey C. Right-left asymmetry of response to visual stimuli in the domestic chick. In: Ingle DI, Goodale MA, Mansfield R, eds. Advances in Analysis of Visual Behavior. Cambridge, MA: MIT Press, 1982; 197-209.
2. Andrew RJ, Tommasi L, Ford N. Motor control by vision and the evolution of cerebral lateralization. Brain Lang 2000; 73: 220-235.
3. Burgess N, Maguire EA, O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002; 35: 625-621.
4. Bunsey M, Eichenbaum H. Conservation of hippocampal memory function in rats and humans. Nature 1996; 379: 255-257.
5. 3H)-proline. J Comp Neurol 1986; 245: 454-470.
6. Clayton NS. Lateralization and unilateral transfer of spatial memory in marsh tits. J Comp Physiol A 1993; 171: 799-806.
7. Clayton NS, Dickinson A. Scrub jays (Aphelocoma coerulescens) remember the relative time of caching as well as the location and content of their caches. Behav Neurosci 1999; 113: 403-416.
8. Colombo M, Broadbent N. Is the avian hippocampus a functional homologue of the mammalian hippocampus? Neurosci Biobehav Rev 2000; 24: 465-484.
9. Deng C, Rogers LJ. Differential contributions of the two visual pathways to functional lateralization in chicks. Behav Brain Res 1997; 87:173-182.
10. Deng C, Rogers LJ. Prehatching visual experience and lateralization in the visual Wulst of the chick. Behav Brain Res 2002;134:375-385.
11. Diekamp B, Prior H, Ioalé P, Odetti F, Güntürkün O, Gagliardo A. Effects of monocular viewing on orientation in an arena at the release site and homing performance in pigeons. Behav Brain Res 2002; 136: 103-111.
12. Eichenbaum H, Stewart C, Morris RGM. Hippocampal representation in place learning. J Neurosci 1990; 10: 3531-3542.
13. Ferbinteanu J, Shapiro ML. Prospective and retrospective memory coding in the hippocampus. Neuron 2003; 40: 1227-1239.
14. th FENS, Lisbon, July 10-14, FENS Abst 2004; vol. 2, A112.23.
15. Gagliardo A, Ioalé P, Bingman VP. Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation. J Neurosci 1999; 19: 311-315.
16. Gagliardo A, Ioalé P, Odetti F, Bingman VP, Siegel JJ, Vallortigara G. Hippocampus and homing pigeons: left and right hemispheric differences in navigational map learning. Eur J Neurosci 2001; 13: 1-9.
17. Gagliardo A, Odetti F, Ioalé P, Bingman VP, Tuttle S, Vallortigara G. Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons. Behav Brain Res 2002; 136: 201-209.
18. Gaston KE. Interocular transfer of pattern discrimination learning in chicks. Brain Res 1984; 310: 213-221.
19. Güntürkün O. Lateralization of visually controlled behavior in pigeons. Physiol Behav 1985; 34: 575-577.
20. Güntürkün O. Avian visual lateralization: a review. NeuroReport 1997; 8: iii-xi.
21. Güntürkün O. Morphological asymmetries of the tectum opticum in the pigeon. Exp Brain Res 1997; 116: 561-566.
22. Güntürkün O. Visual lateralization in birds: From neurotrophins to cognition? Eur J Morphol 1997; 35: 290-302.
23. Güntürkün O, Hahmann U. Visual acuity and hemispheric asymmetries in pigeons. Behav Brain Res 1994; 60: 171-175.
24. Güntürkün O, Kesch S. Visual lateralization during feeding in pigeons. Behav Neurosci 1987; 101: 433-435.
25. Güntürkün O, Hellmann B, Melsbach G, Prior H. Asymmetries of representation in the visual system of pigeons. NeuroReport 1998; 9: 4127-4130.
26. Harris JA, Guglielmotti V, Bentivoglio M. Diencephalic asymmetries. Neurosci Biobehav Rev 1996; 20: 637-643.
27. Hollup SA, Molden S, Donnett JG, Moser MB, Moser EI. Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J Neurosci 2001; 21: 1635-1644.
28. nd, Bingman VP. Spatial response properties of homing pigeon hippocampal neurons: correlations with goal locations, movement between goals, and environmental context in a radial-arm arena. J Comp Physiol A 2004; 190: 1047-1062.
29. Kahn MC, Bingman VP. Lateralization of spatial learning in the avian hippocampal formation. Behav Neurosci 2004; 118: 333-344.
30. Kawakami R, Shinohara Y, Kato Y, Sugiyama H, Shigemoto R, Ito I. Asymmetrical allocation of NMDA receptor e2 subunits in hippocampal circuitry. Science 2003; 300: 990-994.
31. Keysers C, Diekamp B, Gunturkun B. Evidence for physiological asymmetries in the intertectal connections of the pigeon (Columba livia) and their potential role in brain lateralisation. Brain Res 2000; 852: 406-413.
32. Koshiba M, Nakamura S, Deng C, Rogers LJ. Light-dependent development of asymmetry in the ipsilateral and contralateral thalamofugal visual projections of the chick. Neurosci Lett 2003; 336: 81-84.
33. Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL. Hippocampal specialization of food-storing birds. Proc Natl Acad Sci USA 1989; 86: 1388-1392.
34. Lenck-Santini P-P, Save E, Poucet B. Evidence for a relationship between place-cell spatial firing and spatial memory performance. Hippocampus 2001; 11: 377-390.
35. O'Keefe J, Dostrovsky J. The hippocampus as a spatial map: preliminary evidence from unit activity in the freely moving rat. Brain Res 1971; 34: 171-175.
36. Parkinson JK, Murray EA, Mishkin M. A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci 1988; 8: 4159-4167.
37. Prior H, Lingenauber F, Nitschke J, Güntürkün O. Orientation and lateralized cue use in pigeons navigating a large indoor environment. J Exp Biol 2002; 205: 1795-1805.
38. Prior H, Wiltschko R, Stapput K, Güntürkün O, Wiltschko, W. Visual lateralization and homing in pigeons. Behav Brain Res 2004; 154: 301-310.
39. Rashid N, Andrew RJ. Right hemisphere advantage for topographical orientation in the domestic chick. Neuropsychologia 1989; 27: 937-948.
40. Regolin L, Garzotto B, Rugani R, Pagni P, Vallortigara G. Working memory in the chick: parallel and lateralized mechanisms for encoding of object- and position-specific information. Behav Brain Res 2005; 157: 1-9.
41. Rodriguez F, Lopez JC, Vargas, JP, Gomez, Y, Broglio C, Salas C. Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J Neurosci 2002; 22: 2894-2903.
42. Rogers LJ. Behavioral, structural and neurochemical asymmetries in the avian brain: a model system for studying visual development and processing. Neurosci Biobehav Rev 1996; 20: 487-503.
43. Rogers LJ, Anson JM. Lateralisation of function in the chicken fore-brain. Pharmacol Biochem Behav 1979; 10: 679-686.
44. Rogers LJ, Sink HS. Transient asymmetry in the projections of the rostral thalamus to the visual hyperstriatum of the chicken, and reversal of its direction by light exposure. Exp Brain Res 1988; 70: 378-384.
45. Rolls ET. Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 1999; 9: 467-480.
46. Sadananda M, Bischof H-J. c-fos is induced in the hippocampus during consolidation of sexual imprinting in the zebra finch (Taeniopygia guttata). Hippocampus 2004; 14: 19-27.
47. Sharp PE. The Neural Basis of Navigation: Evidence from Single Cell Recording. Boston, MA: Kluwer Academic, 2002.
48. Sherry DF, Vaccarino AL. Hippocampus and memory for food caches in black-capped chickadees. Behav Neurosci 1989; 103: 308-318.
49. Shiflett MW, Smulders TV, Bebedict L, DeVoogd TJ. Reversible inactivation of the hippocampal formation in food storing black-capped chickadees (Poecile atricapillus). Hippocampus 2003; 13: 437-444.
50. Shimizu T, Bowers AN, Budzynski C, Kahn MC, Bingman VP. What does a pigeon brain look like during homing? Selective examination of ZENK expression in the telencephalon of pigeons navigating home. Behav Neurosci 2004; 118: 845-851.
51. Siegel JJ, Nitz D, Bingman VP. Spatial-specificity of single-units in the hippocampal formation of freely moving homing pigeons. Hippocampus 2005; 15: 26-40.
52. 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; in press.
53. Smith ML, Milner B. Right hippocampal impairment in the recall of spatial location: Encoding deficit or rapid forgetting? Neuropsychologia 1989; 27: 71-81.
54. Smulders TV, DeVoogd TJ. Expression of immediate early genes in the hippocampal formation of the black-capped chickadee (Poecile atricapillus) during a food-hoarding task. Behav Brain Res 2000; 114: 39-49.
55. Strasser R, Bingman VP. The effects of hippocampal lesions in homing pigeons on a one-trial food association task. J Comp Physiol A 1999; 185: 583-590.
56. Strasser R, Ehrlinger J, Bingman VP. Transitive behavior in hippocampal-lesioned homing pigeons. Brain Behav Evol 2004; 63: 181-188.
57. Tommasi L, Andrew RJ. The use of viewing posture to control visual processing by lateralised mechanisms. J Exp Biol 2002; 205: 1451-1457.
58. Tommasi L, Gagliardo A, Vallortigara G. Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus. Eur J Neurosci 2003; 17: 1695-1702.
59. Tommasi L, Andrew RJ, Vallortigara G. Eye use in search is determined by the nature of task in the domestic chick (Gallus gallus). Behav Brain Res 2000; 112: 119-126.
60. Ulrich C, Prior H, Duka T, Leshchins'ka I, Valenti P, Güntürkün O, Lipp H-P. Left-hemispheric superiority for visuospatial orientation in homing pigeons. Behav Brain Res 1999; 104: 169-178.
61. Vallortigara G. Comparative neuropsychology of the dual brain: a stroll through animals' left and right perceptual worlds. Brain Lang 2000; 73: 189-219.
62. Vallortigara G, Regolin L, Bortolomiol G, Tommasi L. Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks. Behav Brain Res 1996; 74: 135-143.
63. Watanabe S. Interocular transfer of learning in the pigeon: visuo-motor integration and separation of discriminanda and manipulanda. Behav Brain Res 1986; 19: 227-232.
64. Wiltschko W, Traudt J, Güntürkün O, Prior H, Wiltschko R. Lateralization of magnetic compass orientation in a migratory bird. Nature 2002; 419: 467-470.
65. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000; 27: 623-633.