Directional responding of C57BL/6J mice in the Morris water maze is influenced by visual and vestibular cues and is dependent on the anterior thalamic nuclei

Journal of Neuroscience

Volumn 32, Issue 30, 2012, Pages 10211-10225

  Stackman, Robert W ^a   Lora, Joan C ^a   Williams, Sidney B ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; DISORIENTATION; HIPPOCAMPAL CA1 REGION; HISTOLOGY; MALE; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPATIAL MEMORY; STATE DEPENDENT LEARNING; SWIMMING; THALAMUS ANTERIOR NUCLEUS; TRAINING; VISUAL STIMULATION;

EID: 84864255289     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4868-11.2012     Document Type: Article

References (45)

1. Aggleton JP, Hunt PR, Nagle S, Neave N (1996) The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav Brain Res 81:189-198.
2. Allen TA, Narayanan NS, Kholodar-Smith DB, Zhao Y, Laubach M, Brown TH (2008) Imaging the spread of reversible brain inactivations using fluorescent muscimol. J Neurosci Methods 171:30-38.
3. Béracochéa DJ, Jaffard R (1994) Effects of anterior thalamic lesions on spatial memory in mice. Neuroreport 5:917-920.
4. Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9:182-194.
5. Blodgett HC, McCutchan K, Mathews R (1949) Spatial learning in the Tmaze: the influence of direction, turn, and food location. J Exp Psychol 39:800-809.
6. Calton JL, Stackman RW, Goodridge JP, Archey WB, Dudchenko PA, Taube JS (2003) Hippocampal place cell instability after lesions of the head direction cell network. J Neurosci 23:9719-9731.
7. Clark BJ, Bassett JP, Wang SS, Taube JS (2010) Impaired head direction cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex. J Neurosci 30:5289-5302.
8. DeCoteau WE, Hoang L, Huff L, Stone A, Kesner RP (2004) Effects of hippocampus and medial caudate nucleus lesions on memory for direction information in rats. Behav Neurosci 118:540-545.
9. Eichenbaum H, Stewart C, Morris RG (1990) Hippocampal representation in place learning. J Neurosci 10:3531-3542.
10. Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H (1999) The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23:209-226.
11. Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates. San Diego: Academic.
12. Golob EJ, Taube JS (1997) Head direction cells and episodic spatial information in rats without a hippocampus. Proc Natl Acad Sci U S A 94:7645-7650.
13. 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.
14. Hamilton DA, Akers KG, Weisend MP, Sutherland RJ (2007) How do room and apparatus cues control navigation in the Morris water task? Evidence for distinct contributions to a movement vector. J Exp Psychol Anim Behav Process 33:100-114.
15. Hamilton DA, Akers KG, Johnson TE, Rice JP, Candelaria FT, Sutherland RJ, Weisend MP, Redhead ES (2008) The relative influence of place and direction in the Morris water task. J Exp Psychol Anim Behav Process 34:31-53.
16. Hamilton DA, Akers KG, Johnson TE, Rice JP, Candelaria FT, Redhead ES (2009) Evidence for a shift from place navigation to directional responding in one variant of the Morris water task. J Exp Psychol Anim Behav Process 35:271-278.
17. Jenkins TA, Vann SD, Amin E, Aggleton JP (2004) Anterior thalamic lesions stop immediate early gene activation in selective laminae of the retrosplenial cortex: evidence of covert pathology in rats? Eur J Neurosci 19:3291-3304.
18. Knierim JJ, Hamilton DA (2011) Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. Physiol Rev 91:1245-1279.
19. Maaswinkel H, Jarrard LE, Whishaw IQ (1999) Hippocampectomized rats are impaired in homing by path integration. Hippocampus 9:553-561.
20. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the "cognitive map." Nat Rev Neurosci 7:663-678.
21. Mitchell AS, Dalrymple-Alford JC (2006) Lateral and anterior thalamic lesions impair independent memory systems. Learn Mem 13:388-396.
22. Morris RGM, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
23. Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 31:69-89.
24. Muir GM, Taube JS (2002) The neural correlates of navigation: do head direction and place cells guide spatial behavior? Behav Cogn Neurosci Rev 1:297-317.
25. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford, UK: Clarendon.
26. 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.
27. Pearce JM, Roberts AD, Good M (1998) Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature 396:75-77.
28. Potegal M, Day MJ, Abraham L (1977) Maze orientation, visual and vestibular cues in two-maze spontaneous alternation of rats. Physiol Psychol 5:414-420.
29. Semenov LV, Bures J (1989) Vestibular stimulation disrupts acquisition of place navigation in the Morris water tank task. Behav Neural Biol 51:346-363.
30. Skinner DM, Etchegary CM, Ekert-Maret EC, Baker CJ, Harley CW, Evans JH, Martin GM (2003) An analysis of response, direction, and place learning in an open field and T maze. J Exp Psychol Anim Behav Process 29:3-13.
31. Stackman RW (2010) Behavioral correlates of neuronal activity recorded as single-units. Promises and pitfalls as illustrated by the rodent head direction cell signal. In: Electrophysiological recording methods (Vertes RP, Stackman RW Jr, eds). New York: Springer.
32. 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.
33. Stringer KG, Martin GM, Skinner DM (2005) The effects of hippocampal lesions on response, direction, and place learning in rats. Behav Neurosci 119:946-952.
34. Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70-86.
35. Taube JS (1998) Head direction cells and the neurophysiological basis for a sense of direction. Prog Neurobiol 55:225-256.
36. Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181-207.
37. Tsanov M, Chah E, Vann SD, Reilly RB, Erichsen JT, Aggleton JP, O'Mara SM (2011) Theta-modulated head direction cells in the rat anterior thalamus. J Neurosci 31:9489-9502.
38. van Groen T, Kadish I, Michael Wyss J (2002) Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat. Behav Brain Res 132:19-28.
39. Wallace DG, Hines DJ, Pellis SM, Whishaw IQ (2002) Vestibular information is required for dead reckoning in the rat. J Neurosci 22:10009-10017.
40. Warburton EC, Baird AL, Aggleton JP (1997) Assessing the magnitude of the allocentric spatial deficit associated with complete loss of the anterior thalamic nuclei in rats. Behav Brain Res 87:223-232.
41. Whishaw IQ (1995) A comparison of rats and mice in a swimming pool place task and matching to place task: some surprising differences. Physiol Behav 58:687-693.
42. Whishaw IQ, Tomie J (1996) Of mice and mazes: similarities between mice and rats on dry land but not water mazes. Physiol Behav 60:1191-1197.
43. Wilton LA, Baird AL, Muir JL, Honey RC, Aggleton JP (2001) Loss of the thalamic nuclei for "head direction" impairs performance on spatial memory tasks in rats. Behav Neurosci 115:861-869.
44. Wolff M, Gibb SJ, Cassel JC, Dalrymple-Alford JC (2008) Anterior but not intralaminar thalamic nuclei support allocentric spatial memory. Neurobiol Learn Mem 90:71-80.
45. Yoganarasimha D, Yu X, Knierim JJ (2006) Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J Neurosci 26: 622-631.