Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task

Journal of Neuroscience

Volumn 16, Issue 2, 1996, Pages 823-835

  Gothard, Katalin M ^a   Skaggs, William E ^a   Moore, Kevin M ^a,c   McNaughton, Bruce L ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

CA1; computation; place cells; population code; rat; spatial navigation

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BEHAVIOR THERAPY; HIPPOCAMPUS; LEARNING; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0030031462     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-02-00823.1996     Document Type: Article

References (41)

1. Barnes CA (1988) Spatial learning and memory processes: the search for their neurobiological mechanisms in the rat. Trends Neurosci 11:163-169.
2. Berger TW, Rinaldi PC, Weisz DJ, Thompson RF (1983) Single-unit analysis of different hippocampal cell types during classical conditioning of the nictitating membrane response. J Neurophysiol 50:1197-1219.
3. Biegler R, Morris RGM (1993) Landmark stability is a prerequisite for spatial but not discrimination learning. Nature 361:631-633.
4. Bingman VP, Mench, JA (1990) Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases. Behav Brain Res 40:227-238.
5. Breese CR, Hampson RE, Deadwyler SA (1989) Hippocampal place cells: stereotypy and plasticity. J Neurosci 9:1097-1111.
6. Collett TS, Cartwright BA, Smith BA (1986) Landmark learning and visuo-spatial memories in gerbils. J Comp Physiol 158:835-851.
7. Eichenbaum H, Kuperstein M, Fagan A, Nagode J (1987) Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task. J Neurosci 7:716-732.
8. Eichenbaum H, Wiener SI, Shapiro ML, Cohen NJ (1989) The organization of spatial coding in the hippocampus: a study of the neural ensemble activity. J Neurosci 9:2764-2775.
9. Fox SE, Ranck Jr JB (1981) Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res 41:399-410.
10. Fukuda M, Kobayasni T, Ono T, Tamura R (1992) Effects of learning place significance in rat hippocampal place cells. Soc Neurosci Abstr 18: 1426.
11. Gothard KM, Skaggs WE, Moore KM, McNaughton BL (1994) Behavioral correlates of hippocampal CA1 cells in a landmark navigation task. Soc Neurosci Abstr 20:1207.
12. Jarrard EL (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60:9-26.
13. Jung MW, McNaughton BL (1993) Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165-182.
14. Kubie JL, Ranck Jr JB (1983) Sensory-behavioral correlates in individual hippocampal neurons in three situations: space and context. In: Neurobiology of the hippocampus (Seifert W, ed), pp 433-447. London: Academic.
15. Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4:410-421.
16. Markus EJ, Qin Y, Leonard BJ, Skaggs WE, McNaughton BL, Barnes CA (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15:7079-7094.
17. McNaughton BL, Barnes CA, Gerrard JL, Gothard KM, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1995) Deciphering the hippocampal polyglot: the hippocampus as a path integrator system. J Exp Biol, in press.
18. McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ (1989) Hippocampal granule cells are necessary for spatial learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76:485-496.
19. McNaughton BL, Barnes CA, O'Keefe J (1983a) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 53:41-49.
20. McNaughton BL, Chen LL, Markus EJ (1991) "Dead Reckoning." landmark learning, and the sense of direction: a neurophysiological and computational hypothesis J Cognit Neurosci 3:190-202.
21. McNaughton BL, Knierim JJ, Wilson MA (1994) Vector encoding and the vestibular foundations of spatial cognition: neurophysiological and computational mechanisms. In: The cognitive neurosciences (Gazzaniga M, ed), pp 585-595. Boston: MIT.
22. McNaughton BL, O'Keefe J, Barnes CA (1983b) The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J Neurosci Methods 8:391-397.
23. Mittelstaedt ML, Mittelstaedt H (1980) Homing by path integration in a mammal. Naturwissenschaften 67:566-567.
24. Muller RU, Bostock E, Taube JS, Kubie JL (1994) On the directional firing properties of hippocampal place cells. J Neurosci 14:7235-7251.
25. Muller RU, Kubie JL, Ranck JB Jr (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935-1950.
26. O'Keefe J, Conway DH (1978) Hippocampal place units in the freely- moving rat: why they fire where they fire. Exp Brain Res 31:573-590.
27. O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
28. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford: Clarendon.
29. O'Keefe J, Speakman A (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68:1-27.
30. Otto T, Eichenbaum H (1992) Neuronal activity in the hippocampus during delayed nonmatching to sample performance in rats: evidence for hippocampal processing in recognition memory. Hippocampus 2:323-334.
31. Quirk GJ, Muller RU, Kubie JL (1990) The firing properties of hippocampal place cells in the dark depends on the rat's recent experience. J Neurosci 10:2008-2017.
32. Ranck Jr JB (1973) Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. Exp Neurol 41:461-555.
33. Recce M, Speakman A, O'Keefe J (1991) Place fields of single hippocampal cells are smaller and more spatially localized than you thought. Soc Neurosci Abstr 17:484.
34. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ (1993) An information theoretic approach to deciphering the hippocampal code. In: Progress in neural information processing systems, Vol 5 (Hansen SJ, Cowan JD, Giles CL, eds), pp 1030-1037. San Mateo, CA: Morgan Kaufmann.
35. Thompson LT, Best PJ (1989) Place cells and silent cells in the hippocampus of freely moving rats. J Neurosci 9:2382-2390.
36. Vanderwolf CH, Kramis R, Gillespie LA, Bland BH (1975) Hippocampal rhythmical slow activity and neocortical low voltage fast activity: relations to behavior. In: The hippocampus, Vol. 2, Neurophysiology and behavior (Isaacson RL, Pribram KH, eds), pp 101-128. Plenum: New York.
37. Wan HS, Touretzky DS, Redish AD (1994) Towards a computational theory of rat navigation. In: Proceedings of the 1993 connectionist models summer school (Mozer M, Smolensky P, Touretzky DS, Elman J, Wigend A, eds), pp 11-19. Trenton, NJ: Erlbaum.
38. Wiener SI, Paul CA, Eichenbaum H (1989) Spatial and behavioral correlates of hippocampal neuronal activity. J Neurosci 9:2737-2763.
39. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058.
40. Worden R (1992) Navigation by fragment fitting: a theory of hippocampal function. Hippocampus 2:165-187.
41. Young BJ, Fox GD, Eichenbaum H (1994) Correlates of hippocampal complex-spike activity in rats performing a nonspatial radial maze task. J Neurosci 14:6553-6563.