Mammillothalamic tract lesions disrupt dead reckoning in the rat

European Journal of Neuroscience

Volumn 33, Issue 2, 2011, Pages 371-381

  Winter, Shawn S ^a   Wagner, Steven J ^a   McMillin, Jeffery L ^a   Wallace, Douglas G ^a  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

Limbic system; Mammillary bodies; Path integration; Spatial orientation; Translational neuroscience

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; FEMALE; FOOD HOARDING; LIMBIC SYSTEM; MAMILLOTHALAMIC TRACT LESION; MAZE TEST; NERVE LESION; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL ORIENTATION; WATER MAZE;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MAMILLARY BODIES; MAZE LEARNING; MOVEMENT; NEURAL PATHWAYS; ORIENTATION; RATS; RATS, LONG-EVANS; SPACE PERCEPTION; SPATIAL BEHAVIOR;

EID: 78651423867     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07504.x     Document Type: Article

References (63)

1. Allen, K., Potvin, O., Thibaudeau, G., Doré, F.Y. & Goulet, S. (2007) Processing idiothetic cues to remember visited locations: hippocampal and vestibular contributions to radial-arm maze performance. Hippocampus, 17, 642-653.
2. Barlow, J.S. (1964) Inertial navigation as a basis for animal navigation. J. Theor. Biol., 6, 76-117.
3. Bassett, J.P., Tullman, M.L. & Taube, J.S. (2007) Lesions of the tegmentomammillary circuit in the head direction system disrupt the head direction signal in the anterior thalamus. J. Neurosci., 27, 7564-7577.
4. Batschelet, E. (1981) Circular Statistics in Biology. Academic Press, London.
5. Béracochéa, D.J., Micheau, J. & Jaffard, R. (1995) Alteration of cortical and hippocampal cholinergic activities following lesion of the mammillary bodies in mice. Brain Res., 670, 53-58.
6. Biegler, R. & Morris, R. (1996) Landmark stability: studies exploring whether the perceived stability of the environment influences spatial representation. J. Exp. Biol., 199(Pt 1), 187-193.
7. Blair, H.T. & Sharp, P.E. (1996) Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat. Behav. Neurosci., 110, 643-660.
8. Blair, H.T., Cho, J. & Sharp, P.E. (1998) Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study. Neuron, 21, 1387-1397.
9. Blair, H.T., Cho, J. & Sharp, P.E. (1999) The anterior thalamic head-direction signal is abolished by bilateral but not unilateral lesions of the lateral mammillary nucleus. J. Neurosci., 19, 6673-6683.
10. Brandt, T., Schautzer, F., Hamilton, D.A., Brüning, R., Markowitsch, H.J., Kalla, R., Darlington, C., Smith, P. & Strupp, M. (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain, 128(Pt 11), 2732-2741.
11. Clark, B.J., Bassett, J.P., Wang, S.S. & Taube, J.S. (2010) Impaired head direction cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex. J. Neurosci., 30, 5289-5302.
12. Darwin, C. (1873) Origin of certain insects. Nature, 7, 417-418.
13. Etienne, A.S. & Jeffery, K.J. (2004) Path integration in mammals. Hippocampus, 14, 180-192.
14. Etienne, A.S., Maurer, R., Saucy, F. & Teroni, E. (1986) Short distance homing in the golden hamster after a passive outward journey. Anim. Behav., 34, 696-715.
15. Field, T.D., Rosenstock, J., King, E.C. & Greene, E. (1978) Behavioral role of the mammillary efferent system. Brain Res. Bull., 3, 451-456.
16. Frohardt, R.J., Bassett, J.P. & Taube, J.S. (2006) Path integration and lesions within the head direction cell circuit: comparison between the roles of the anterodorsal thalamus and dorsal tegmental nucleus. Behav. Neurosci., 120, 135-149.
17. Gallistel, C.R. (1990) The Organization of Learning. MIT, Cambridge.
18. Goodridge, J.P. & Taube, J.S. (1997) Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J. Neurosci., 17, 9315-9330.
19. Goodridge, J.P., Dudchenko, P.A., Worboys, K.A., Golob, E.J. & Taube, J.S. (1998) Cue control and head direction cells. Behav. Neurosci., 112, 749-761.
20. Gupta, A.S., van der Meer, M.A., Touretzky, D.S. & Redish, A.D. (2009) Hippocampal replay is not a simple function of experience. Neuron, 65, 695-705.
21. Hamilton, D.A., Rosenfelt, C.S. & Whishaw, I.Q. (2004) Sequential control of navigation by locale and taxon cues in the Morris water task. Behav. Brain Res., 154, 385-397.
22. Hamilton, D.A., Johnson, T.E., Redhead, E.S. & Verney, S.P. (2009) Control of rodent and human spatial navigation by room and apparatus cues. Behav. Processes, 81, 154-169.
23. Harker, KT & Whishaw, IQ (2002) Place and matching-to-place spatial learning affected by rat inbreeding (Dark-Agouti, Fischer 344) and albinism (Wistar, Sprague-Dawley) but not domestication (wild rat vs Long-Evans, Fischer-Norway). Behav. Brain Res., 134, 467-477.
24. Kirk, I.J. (1997) Supramammillary neural discharge patterns and hippocampal EEG. Brain Res. Bull., 42, 23-26.
25. Kirk, I.J., Oddie, S.D., Konopacki, J. & Bland, B.H. (1996) Evidence for differential control of posterior hypothalamic, supramammillary, and medial mammillary theta-related cellular discharge by ascending and descending pathways. J. Neurosci., 16, 5547-5554.
26. Knierim, J.J., Kudrimoti, H.S. & McNaughton, B.L. (1995) Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol., 80, 425-446.
27. Maaswinkel, H., Jarrard, L.E. & Whishaw, I.Q. (1999) Hippocampectomized rats are impaired in homing by path integration. Hippocampus, 9, 553-561.
28. Manns, J.R. & Eichenbaum, H. (2009) A cognitive map for object memory in the hippocampus. Learn Mem., 16, 616-624.
29. Martin, M.M. & Wallace, D.G. (2007) Selective hippocampal cholinergic deafferentation impairs self-movement cue use during a food hoarding task. Behav. Brain Res., 183, 78-86.
30. Means, L.W., Alexander, S.R. & O' Neal, M.F. (1992) Those cheating rats: male and female rats use odor trails in a water-escape "working memory" task. Behav. Neural Biol., 58, 144-151.
31. Morris, R.G., Garrud, P., Rawlins, J.N. & O'Keefe, J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-683.
32. Murphy, J.J. (1873) Instinct: a mechanical analogy. Nature, 7, 483.
33. Neave, N., Nagle, S. & Aggleton, J.P. (1997) Evidence for the involvement of the mammillary bodies and cingulum bundle in allocentric spatial processing by rats. Eur. J. Neurosci., 9, 941-955.
34. Neitz, J. & Jacobs, G.H. (1986) Reexamination of spectral mechanisms in the rat (Rattus norvegicus). J. Comp. Psychol., 100, 21-29.
35. O'Keefe, J. & Nadel, L. (1978) The Hippocampus as a Cognitive Map. Clarendon, Oxford.
36. Pearce, J.M., Roberts, A.D. & Good, M. (1998) Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature, 396, 75-77.
37. Prusky, G.T., Harker, K.T., Douglas, R.M. & Whishaw, I.Q. (2002) Variation in visual acuity within pigmented, and between pigmented and albino rat strains. Behav. Brain Res., 136, 339-348.
38. Russell, N.A., Horii, A., Smith, P.F., Darlington, C.L. & Bilkey, D.K. (2003) Bilateral peripheral vestibular lesions produce long-term changes in spatial learning in the rat. J. Vestib. Res., 13, 9-16.
39. Schautzer, F., Hamilton, D., Kalla, R., Strupp, M. & Brandt, T. (2003) Spatial memory deficits in patients with chronic bilateral vestibular failure. Ann. N Y Acad. Sci., 1004, 316-324.
40. Semenov, L.V. & Bures, J. (1989) Vestibular stimulation disrupts acquisition of place navigation in the Morris water tank task. Behav. Neural Biol., 51, 346-363.
41. Stackman, R.W. & Taube, J.S. (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J. Neurosci., 17, 4349-4358.
42. Sutherland, R.J. & Rodriguez, A.J. (1989) The role of the fornix/fimbria and some related subcortical structures in place learning and memory. Behav. Brain Res., 32, 265-277.
43. Sziklas, V. & Petrides, M. (1993) Memory impairments following lesions to the mammillary region of the rat. Eur. J. Neurosci., 5, 525-540.
44. Sziklas, V. & Petrides, M. (2000) Selectivity of the spatial learning deficit after lesions of the mammillary region in rats. Hippocampus, 10, 325-328.
45. Taube, J.S., Muller, R.U. & Ranck, J.B. (1990b) Head-direction cells recorded from the postsubiculum in freely moving rats II. Effects of environmental manipulations. J. Neurosci., 10, 436-447.
46. Tsivilis, D., Vann, S.D., Denby, C., Roberts, N., Mayes, A.R., Montaldi, D. & Aggleton, J.P. (2008) A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat. Neurosci., 11, 834-842.
47. Van der Werf, Y.D., Scheltens, P., Lindeboom, J., Witter, M.P., Uylings, H.B. & Jolles, J. (2003) Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions. Neuropsychologia, 41, 1330-1344.
48. Vann, S.D. (2005) Transient spatial deficit associated with bilateral lesions of the lateral mammillary nuclei. Eur. J. Neurosci., 21, 820-824.
49. Vann, S.D. (2010) Re-evaluating the role of the mammillary bodies in memory. Neuropsychologia, 48, 2316-2327.
50. Vann, S.D. & Aggleton, J.P. (2003) Evidence of a spatial encoding deficit in rats with lesions of the mammillary bodies or mammillothalamic tract. J. Neurosci., 23, 3506-3514.
51. Vann, S.D. & Aggleton, J.P. (2004) The mammillary bodies: two memory systems in one? Nat. Rev. Neurosci., 5, 35-44.
52. Vann, S.D. & Albasser, M.M. (2009) Hippocampal, retrosplenial, and prefrontal hypoactivity in a model of diencephalic amnesia: evidence towards an interdependent subcortical-cortical memory network. Hippocampus, 19, 1090-1102.
53. Vargha-Khadem, F., Gadian, G.D., Watkins, K.E., Connelly, A., Van Paesschen, W. & Mishkin, M. (1997) Differential effects of early hippocampal pathology on episodic and semantic memory. Science, 277, 376-380.
54. Wallace, D.G., Gorny, B. & Whishaw, I.Q. (2002a) Rats can track odors, other rats, and themselves: implications for the study of spatial behavior. Behav. Brain Res., 131, 185-192.
55. Wallace, D.G., Hines, D.J., Pellis, S.M. & Whishaw, I.Q. (2002b) Vestibular information is required for dead reckoning in the rat. J. Neurosci., 22, 10009-10017.
56. Wallace, D.G., Martin, M.M. & Winter, S.S. (2008) Fractionating dead reckoning: role of the compass, odometer, logbook, and home base establishment in spatial orientation. Naturwissenschaften, 95, 1011-1026.
57. Whishaw, I.Q. (1985) Formation of a place learning-set by the rat: a new paradigm for neurobehavioral studies. Physiol. Behav., 35, 139-143.
58. Whishaw, I.Q. (1998) Place learning in hippocampal rats and the path integration hypothesis. Neurosci. Biobehav. Rev., 22, 209-220.
59. Whishaw, I.Q. & Tomie, J. (1997) Piloting and dead reckoning dissociated by fimbria-fornix lesions in a rat food carrying task. Behav. Brain Res., 89, 87-97.
60. Whishaw, I.Q. & Wallace, D.G. (2003) On the origins of autobiographical memory. Behav. Brain Res., 138, 113-119.
61. Whishaw, I.Q., Maaswinkel, H., Gonzalez, C.L. & Kolb, B. (2001) Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions. Behav. Brain Res., 118, 67-76.
62. Wolbers, T., Wiener, J.M. & Mallot HA, B.C. (2007) Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans. J. Neurosci., 27, 9408-9416.
63. Zheng, Y., Goddard, M., Darlington, C.L. & Smith, P.F. (2007) Bilateral vestibular deafferentation impairs performance in a spatial forced alternation task in rats. Hippocampus, 17, 253-256.