Deciphering the hippocampal polyglot: The hippocampus as a path integration system

Journal of Experimental Biology

Volumn 199, Issue 1, 1996, Pages 173-185

  Mcnaughton, B L ^a   Barnes, C A ^a   Gerrard, J L ^a   Gothard, K ^a   Jung, M W ^a   Knierim, J J ^a   Kudrimoti, H ^a   Qin, Y ^a   Skaggs, W E ^a   Suster, M ^a   Weaver, K L ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Cognitive maps; Dead reckoning; Head direction cells; Navigation; Place cells

Indexed keywords

ANIMAL; COGNITION; DEPTH PERCEPTION; HEAD; HIPPOCAMPUS; MOVEMENT (PHYSIOLOGY); NERVE CELL PLASTICITY; PHYSIOLOGY; RAT; REVIEW; VISUAL SYSTEM;

ANIMALS; COGNITION; HEAD; HIPPOCAMPUS; MOVEMENT; NEURONAL PLASTICITY; RATS; SPACE PERCEPTION; VISUAL PATHWAYS;

EID: 0000876225     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. ALYAN, S. AND JANDER, R. (1994). Short-range homing in the house mouse, Mus musculus: Stages in the learning of directions. Anim. Behav. 48, 285-298.
2. AMIT, D. J. (1989). Modeling Brain Function: The World of Attractor Networks. New York: Cambridge University Press.
3. BARLOW, J. S. (1964). Inertial navigation as a basis for animal navigation. J. theor. Biol. 6, 76-117.
4. BOSTOCK, E., MULLER, R. U. AND KUBIE, J. L. (1991). Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1, 193-206.
5. BREESE, C. R., HAMPSON, R. E. AND DEADWYLER, S. A. (1989). Hippocampal place cells, stereotypy and plasticity. J. Neurosci. 9, 1097-1111.
6. CHEN, L. L., LIN, L.-H., BARNES, C. A. AND MCNAUGHTON, B. L. (1994a). Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp. Brain Res. 101, 24-34.
7. CHEN, L. L., LIN, L.-H., GREEN, E. J., BARNES, C. A. AND MCNAUGHTON, B. L. (1994b). Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp. Brain Res. 101, 8-23.
8. ETIENNE, A. S. (1987). The control of short-distance homing in the golden hamster. In Cognitive Processes in Spatial Orientation in Animal and Man (ed. P. Ellen and C. Thinus-Blanc), pp. 223-251. Dordrecht, The Netherlands: Martinus Nijhoff.
9. FOSTER, T. C., CASTRO, C. A. AND MCNAUGHTON, B. L. (1989). Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. Science 244, 1580-1582.
10. FUKUDA, M., KOBAYASHI, T., ONO, T. AND TAMURA, R. (1992). Effects of learning place significance on rat hippocampal place cells. Soc. Neurosci. Abstr. 18, 1426.
11. GOTHARD, K. M., SKAGGS, W. E. AND MCNAUGHTON, B. L. (1995). Binding of hippocampal CAl neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci. (in press).
12. HEBB, D. O. (1949). The Organization of Behavior. New York: Wiley.
13. HILL, A. J. (1978). First occurrence of hippocampal spatial firing in a new environment. Exp. Neurol. 62, 282-297.
14. HOPFIELD, J. J. (1982). Neural networks and physical systems with emergent collective computational abilities. Proc. natn. Acad. Sci. U.S.A. 79, 2554-2558.
15. JUNG, M. W. AND MCNAUGHTON, B. L. (1993). Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3, 165-182.
16. JUNG, M. W., WIENER, S. I. AND MCNAUGHTON, B. L. (1994). Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14, 7347-7356.
17. KNIERIM, J. J., KUDRIMOTI, H. S. AND MCNAUGHTON, B. L. (1995a). Hippocampal place fields, the internal compass and the learning of landmark stability. J. Neurosci. 15, 1648-1659.
18. KNIERIM, J. J., KUDRIMOTI, H. S., SKAGGS, W. E. AND MCNAUGHTON, B. L. (1995b). The interaction between vestibular cues and visual landmark learning in spatial navigation. Ann. N. Y. Acad. Sci. (in press).
19. KUBIE, J. L. AND RANCK, J. B. J. (1983). Sensory-behavioral correlates in individual hippocampus neurons in three situations: space and context. In Neurobiology of the Hippocampus (ed. W. Seifert), pp. 443-447. New York: Academic Press.
20. KUDRIMOTI, H. S., MCNAUGHTON, B. L., BARNES, C. A. AND SKAGGS, W. E. (1995). Recent experience strengthens preexisting correlationships between hippocampal neurons during sleep. Soc. Neurosci. Abstr. 21 (in press).
21. MARKUS, E. J., BARNES, C. A., MCNAUGHTON, B. L., GLADDEN, V. L. AND SKAGGS, W. E. (1994). Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input. Hippocampus 4, 410-421.
22. MARKUS, E. J., QIN, Y., LEONARD, B. J., SKAGGS, W. E., MCNAUGHTON, B. L. AND BARNES, C. A. (1995). Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. (in press).
23. MARR, D. (1971). Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B 262, 23-81.
24. MCCLELLAND, J. L., MCNAUGHTON, B. L. AND O'REILLY, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psych. Rev. 102, 419-457.
25. MCNAUGHTON, B. L., BARNES, C. A. AND O'KEEFE, J. (1983). The contributions of position, direction and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 52, 41-49.
26. McNAUGHTON, B. L., CHEN, L. L. AND MARKUS, E. J. (1991). 'Dead Reckoning,' landmark learning and the sense of direction: A neurophysiological and computational hypothesis. J. cog. Neurosci. 3, 190-202.
27. MCNAUGHTON, B. L., KNIERIM, J. J. AND WILSON, M. A. (1994). Vector encoding and the vestibular foundations of spatial cognition. In The Cognitive Neurosciences (ed. M. Gazzaniga), pp. 585-595. Boston: MIT Press.
28. MCNAUGHTON, B. L., LEONARD, B. AND CHEN, L. (1989). Cortical-hippocampal interactions and cognitive mapping: A hypothesis based on reintegration of the parietal and inferotemporal pathways for visual processing. Psychobiol. 17, 230-235.
29. MCNAUGHTON, B. L. AND MORRIS, R. G. M. (1987). Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10, 408-415.
30. MCNAUGHTON, B. L. AND NADEL, L. (1989). Hebb-Marr networks and the neurobiological representation of action in space. In Neuroscience and Connectionist Theory (ed. M. A. Gluck and D. E. Rumelhart), pp. 1-63. Hillsdale: Lawrence Erlbaum Associates.
31. MITTELSTAEDT, M. L. AND MITTELSTAEDT, H. (1980). Homing by path integration in a mammal. Naturwissenschaften 67, 566-567.
32. MIZUMORI, S. J. Y. AND WILLIAMS, J. D. (1993). Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J. Neurosci. 13, 4015-4028.
33. MULLER, R. U. AND KUBIE, J. L. (1987). The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 77, 1951-1968.
34. MULLER, R. U., KUBIE, J. L. AND RANCK, J. B., JR (1987). Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 77, 1935-1950.
35. NADEL, L., WILNER, J. AND KURZ, E. M. (1985). Cognitive maps and environmental context. In Context and Learning (ed. P. Balsam and A. Tomie), pp. 385-406. Hillsdale, NJ: Lawrence Earlbaum Associates.
36. O'KEEFE, J. (1976). Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 8-109.
37. O'KEEFE, J. AND DOSTROVSKY, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175.
38. O'KEEFE, J. AND NADEL, L. (1978). The Hippocampus as a Cognitive Map. Oxford: Clarendon Press.
39. O'KEEFE, J. AND SPEAKMAN, A. (1987). Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res. 68, 1-27.
40. PAVLIDES, C. AND WINSON, J. (1989). Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J. Neurosci. 9, 2907-2918.
41. QUIRK, G. J., MULLER, R. U. AND KUBIE, J. L. (1990). The firing of hippocampal place cells in the dark depends on the rat's recent experience. J. Neurosci. 10, 2008-2017.
42. RANCK, J. B., JR (1984). Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. Soc. Neurosci. Abstr. 10, 599.
43. SHARP, P. E. AND GREEN, C. (1993). Spatial correlates of firing patterns of single cells in the subiculum of the freely-moving rat. J. Neurosci. 14, 2339-2356.
44. SHARP, P. E., KUBIE, J. L. AND MULLER, R. U. (1990). Firing properties of hippocampal neurons in a visually symmetrical environment: contributions of multiple sensory cues and mnemonic properties. J. Neurosci. 10. 3093-3105.
45. SHEN, B. AND MCNAUGHTON, B. L. (1994). Simulation of the spontaneous reactivation of experience-specific hippocampal cell assemblies during sleep. Soc. Neurosci. Abstr. 20, 1206.
46. SKAGGS, W. E. (1995). Relations between the theta rhythm and activity patterns of hippocampal neurons. PhD dissertation, Program in Neuroscience, University of Arizona, Tucson, USA.
47. SKAGGS, W. E., KNIERIM, J. J., KUDRIMOTI, H. S. AND MCNAUGHTON, B. L. (1995). A model of the neural basis of the rat's sense of direction. In Advances in Neural Information Processing Systems, vol. 7 (ed. G. Tesauro, D. Touretzky and T. Leen), pp. 173-180. Cambridge: MIT Press.
48. SQUIRE, L. R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys and humans. Psychol. Rev. 99, 195-231.
49. TAUBE, J. S. (1995). Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15, 70-86.
50. TAUBE, J. S., MULLER, R. U. AND RANCK, J. B. J. (1987). A quantitative analysis of head-direction cells in the postsubiculum. J. Neurosci. 13, 1332.
51. THINUS-BLANC, C., BOUZOUBA, L., CHAIX, K., CHAPUIS, N., DURUP, M. AND POUCET, B. (1987). A study of spatial parameters encoded during exploration in hamsters. J. exp. Psychol.: Anim. Behav. Proc. 13, 418-427.
52. TREVES, A. AND ROLLS, E. T. (1994). A computational analysis of the role of the hippocampus in memory. Hippocampus 4, 373-391.
53. WAN, H. S., TOURETZKY, D. S. AND REDISH, A. D. (1994). Towards a computational theory of rat navigation. In Proceedings of the 1993 Connectionist Models Summer School (ed. M. Mozer, P. Smolensky, D. S. Touretzky, J. Elman and A. Wigend), pp. 11-19. Hillsdale: Lawrence Erlbaum Associates.
54. WILSON, M. A. AND MCNAUGHTON, B. L. (1993). Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058.
55. WILSON, M. A. AND MCNAUGHTON, B. L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-679.
56. WORDEN, R. (1992). Navigation by fragment fitting: a theory of hippocampal function. Hippocampus 2, 165-188.