Directional learning, but no spatial mapping by rats performing a navigational task in an inverted orientation

Neurobiology of Learning and Memory

Volumn 93, Issue 4, 2010, Pages 495-505

  Valerio, Stephane ^a   Clark, Benjamin J ^a   Chan, Jeremy H M ^a   Frost, Carlton P ^a   Harris, Mark J ^a   Taube, Jeffrey S ^a  

^a Dartmouth College   (United States)

Author keywords

Head direction cells; Spatial navigation; Spatial task; Vestibular system

Indexed keywords

ACCURACY; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ESCAPE BEHAVIOR; FEMALE; HEAD POSITION; LOCOMOTION; MENTAL PERFORMANCE; NONHUMAN; RAT; SPATIAL DISCRIMINATION; SPATIAL ORIENTATION;

ANALYSIS OF VARIANCE; ANIMALS; CUES; FEMALE; LEARNING; MAZE LEARNING; MEMORY; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TESTS; OLFACTORY PERCEPTION; PHOTIC STIMULATION; RATS; RATS, LONG-EVANS; SPACE PERCEPTION; TIME FACTORS; VISUAL PERCEPTION;

EID: 77952554516     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2010.01.007     Document Type: Article

References (51)

1. Aggleton J.P., Hunt P.R., Nagle S., Neave N. The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behavioural Brain Research 1996, 81(1-2):189-198.
2. Aguirre G.K., Zarahn E., D'Esposito M. Neural components of topographical representation. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(3):839-846.
3. Alstott J., Timberlake W. Effects of rat sex differences and lighting on locomotor exploration of a circular open field with free-standing central corners and without peripheral walls. Behavioural Brain Research 2009, 196(2):214-219.
4. Aoki H., Ohno R., Yamaguchi T. The effect of the configuration and the interior design of a virtual weightless space station on human spatial orientation. Acta Astronomica 2005, (56):1005-1016.
5. Aoki H., Ohno R., Yamguchi T. A study of spatial orientation in a virtual weightless environment. Part 2 causes of spatial cognition errors. Journal of Architecture, Planning and Environmental Engineering 2003, (563):85-92.
6. Bassett J.P., Tullman M.L., Taube J.S. Lesions of the tegmentomammillary circuit in the head direction system disrupt the head direction signal in the anterior thalamus. Journal of Neuroscience 2007, 27(28):7564-7577.
7. Calton J.L., Taube J.S. Degradation of head direction cell activity during inverted locomotion. Journal of Neuroscience 2005, 25(9):2420-2428.
8. Clark B.J., Hamilton D.A., Whishaw I.Q. Motor activity (exploration) and formation of home bases in mice (C57BL/6) influenced by visual and tactile cues: Modification of movement distribution, distance, location, and speed. Physiology & Behavior 2006, 87(4):805-816.
9. Eichenbaum H., Fagan A., Mathews P., Cohen N.J. Hippocampal system dysfunction and odor discrimination learning in rats: Impairment or facilitation depending on representational demands. Behavioral Neuroscience 1988, 102(3):331-339.
10. Eichenbaum H., Mathews P., Cohen N.J. Further studies of hippocampal representation during odor discrimination learning. Behavioral Neuroscience 1989, 103(6):1207-1216.
11. Eichenbaum H., Stewart C., Morris R.G. Hippocampal representation in place learning. Journal of Neuroscience 1990, 10(11):3531-3542.
12. Eilam D. Locomotor activity in common spiny mice (Acomys cahirinuse): The effect of light and environmental complexity. BMC Ecology 2004, 4(1):16.
13. Ekstrom A.D., Kahana M.J., Caplan J.B., Fields T.A., Isham E.A., Newman E.L., et al. Cellular networks underlying human spatial navigation. Nature 2003, 425(6954):184-188.
14. Gold P.E. Coordination of multiple memory systems. Neurobiology of Learning and Memory 2004, 82(3):230-242.
15. Golob E.J., Stackman R.W., Wong A.C., Taube J.S. On the behavioral significance of head direction cells: Neural and behavioral dynamics during spatial memory tasks. Behavioral Neuroscience 2001, 115(2):285-304.
16. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436(7052):801-806.
17. Hamilton D.A., Akers K.G., Johnson T.E., Rice J.P., Candelaria F.T., Sutherland R.J., et al. The relative influence of place and direction in the Morris water task. Journal of Experimental Psychology - Animal Behavior Processes 2008, 34(1):31-53.
18. Hamilton, D. A., Clark, B. J., Rice, J., Johnson, T., Akers, K. G., & Taube, J. S. (2009). Dorsal tegmental nucleus lesions disrupt control of navigation by distal visual cues in cued, directional, and place variants of the Morris water task. In: Paper presented at the annual meeting of society for neuroscience, Chicago.
19. Hartley T., Maguire E.A., Spiers H.J., Burgess N. The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37(5):877-888.
20. Knowlton B.J., Mangels J.A., Squire L.R. A neostriatal habit learning system in humans. Science 1996, 273(5280):1399-1402.
21. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S., Frith C.D., O'Keefe J. Knowing where and getting there: A human navigation network. Science 1998, 280(5365):921-924.
22. McDonald R.J., White N.M. A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience 1993, 107(1):3-22.
23. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
24. Nasello A.G., Machado C., Bastos J.F., Felicio L.F. Sudden darkness induces a high activity-low anxiety state in male and female rats. Physiology & Behavior 1998, 63(3):451-454.
25. O'Keefe J. Place units in the hippocampus of the freely moving rat. Experimental Neurology 1976, 51(1):78-109.
26. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research 1971, 34(1):171-175.
27. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Oxford University Press, Oxford, England.
28. Oman C.M. Spatial orientation and navigation in microgravity. Spatial processing in navigation, imagery and perception 2007, Springer, New-York. F.W. Mast, L. Jäncke (Eds.).
29. Oman C.M., Shebilske W.L., Richards J.T., Tubre T.C., Beall A.C., Natapoff A. Three dimensional spatial memory and learning in real and virtual environments. Spatial Cognition and Computation 2002, (2):355-372.
30. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65(1):65-72.
31. Peruch P., Borel L., Magnan J., Lacour M. Direction and distance deficits in path integration after unilateral vestibular loss depend on task complexity. Brain Research Cognitive Brain Research 2005, 25(3):862-872.
32. Poldrack R.A., Clark J., Pare-Blagoev E.J., Shohamy D., Creso Moyano J., Myers C., et al. Interactive memory systems in the human brain. Nature 2001, 414(6863):546-550.
33. Ragozzino K.E., Leutgeb S., Mizumori S.J. Dorsal striatal head direction and hippocampal place representations during spatial navigation. Experimental Brain Research 2001, 139(3):372-376.
34. Richards J.T., Oman C.M., Shebilske W.L., Beall A.C., Liu A.M., Natapoff A. Training, transfer and retention of three-dimensional spatial memory in virtual environments. Journal of Vestibular Research 2003, 12:223-238.
35. Skinner D.M., Etchegary C.M., Ekert-Maret E.C., Baker C.J., Harley C.W., Evans J.H., et al. An analysis of response, direction, and place learning in an open field and T maze. Journal of Experimental Psychology - Animal Behavior Processes 2003, 29(1):3-13.
36. Squire L.R. Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory 2004, 82(3):171-177.
37. Stackman R.W., Golob E.J., Bassett J.P., Taube J.S. Passive transport disrupts directional path integration by rat head direction cells. Journal of Neurophysiology 2003, 90(5):2862-2874.
38. Stackman R.W., Tullman M.L., Taube J.S. Maintenance of rat head direction cell firing during locomotion in the vertical plane. Journal of Neurophysiology 2000, 83(1):393-405.
39. Steffenach H.A., Witter M., Moser M.B., Moser E.I. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 2005, 45(2):301-313.
40. Stringer K.G., Martin G.M., Skinner D.M. The effects of hippocampal lesions on response, direction, and place learning in rats. Behavioral Neuroscience 2005, 119(4):946-952.
41. Sziklas V., Petrides M. The effects of lesions to the anterior thalamic nuclei on object-place associations in rats. European Journal of Neuroscience 1999, 11(2):559-566.
42. Taube J.S. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. Journal of Neuroscience 1995, 15(1 Pt 1):70-86.
43. Taube J.S., Kesslak J.P., Cotman C.W. Lesions of the rat postsubiculum impair performance on spatial tasks. Behavioral and Neural Biology 1992, 57(2):131-143.
44. Taube J.S., Muller R.U., Ranck J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. Journal of Neuroscience 1990, 10(2):420-435.
45. Taube J.S., Stackman R.W., Calton J.L., Oman C.M. Rat head direction cell responses in zero-gravity parabolic flight. Journal of Neurophysiology 2004, 92(5):2887-2997.
46. Tolman E.C., Ritchie B.F., Kalish D. Studies in spatial learning. I. Orientation and the short-cut. Journal of Experimental Psychology 1946, 36:13-24.
47. Vidal M., Amorim M.A., Berthoz A. Navigating in a virtual three-dimensional maze: How do egocentric and allocentric reference frames interact?. Brain Research Cognitive Brain Research 2004, 19(3):244-258.
48. Warburton E.C., Baird A.L., Aggleton J.P. Assessing the magnitude of the allocentric spatial deficit associated with complete loss of the anterior thalamic nuclei in rats. Behavioural Brain Research 1997, 87(2):223-232.
49. Wiener S.I. Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. Journal of Neuroscience 1993, 13(9):3802-3817.
50. Wolff M., Gibb S.J., Cassel J.C., Dalrymple-Alford J.C. Anterior but not intralaminar thalamic nuclei support allocentric spatial memory. Neurobiology of Learning and Memory 2008, 90(1):71-80.
51. Yin H.H., Ostlund S.B., Knowlton B.J., Balleine B.W. The role of the dorsomedial striatum in instrumental conditioning. European Journal of Neuroscience 2005, 22(2):513-523.