Different CA1 and CA3 representations of novel routes in a shortcut situation

Journal of Neuroscience

Volumn 28, Issue 29, 2008, Pages 7324-7333

  Alvernhe, Alice ^a   Van Cauter, Tiffany ^a   Save, Etienne ^a   Poucet, Bruno ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Hippocampus; Place cells; Rat; Spatial cognition; Spatial processing; Unit recordings

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; HIPPOCAMPUS; KINEMATICS; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL DISCRIMINATION; SPATIAL ORIENTATION; ACTION POTENTIAL; ANIMAL; BEHAVIOR; COMPARATIVE STUDY; CYTOLOGY; DEPTH PERCEPTION; HISTOLOGY; LONG EVANS RAT; NERVE CELL; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; HIPPOCAMPUS; MALE; MAZE LEARNING; NEURONS; RATS; RATS, LONG-EVANS; SPACE PERCEPTION; SPATIAL BEHAVIOR;

EID: 49049118724     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1909-08.2008     Document Type: Article

References (58)

1. Agster KL, Fortin NJ, Eichenbaum H (2002) The hippocampus and disambiguation of overlapping sequences. J Neurosci 22:5760-5768.
2. Ainge JA, Tamosiunaite M, Woergoetter F, Dudchenko PA (2007) Hippocampal CA1 place cells encode intended destination on a maze with multiple choice points. J Neurosci 27:9769-9779.
3. Barry C, Burgess N (2007) Learning in a geometric model of place cell firing. Hippocampus 17:786-800.
4. Battaglia FP, Treves A (1998) Attractor neural networks storing multiple space representations: a model for hippocampal place fields. Phys Rev E 58:7738-7753.
5. Bower MR, Euston DR, McNaughton BL (2005) Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. J Neurosci 25:1313-1323.
6. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243-2246.
7. Dragoi G, Buzsáki G (2006) Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50:145-157.
8. Fenton AA, Csizmadia G, Muller RU (2000) Conjoint control of hippocampal place cell firing by two visual stimuli. I. The effects of moving the stimuli on firing field positions. J Gen Physiol 116:191-209.
9. Ferbinteanu J, Shapiro ML (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40:1227-1239.
10. Fortin NJ, Agster KL, Eichenbaum HB (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5:458-462.
11. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680-683.
12. Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169-178.
13. Gaussier P, Revel A, Banquet JP, Babeau V (2002) From view cells and place cells to cognitive map learning: processing stages of the hippocampal system. Biol Cybern 86:15-28.
14. Gilbert PE, Kesner RP (2006) The role of dorsal CA3 hippocampal subregion in spatial working memory and pattern separation. Behav Brain Res 169:142-149.
15. Gold AE, Kesner RP (2005) The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15:808-814.
16. Gothard KM, Skaggs WE, Moore KM, McNaughton BL (1996) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci 16:823-835.
17. Hartley T, Burgess N, Lever C, Cacucci F, O'Keefe J (2000) Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10:369-379.
18. Hetherington PA, Shapiro ML (1997) Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. Behav Neurosci 111:20-34.
19. Jeffery KJ, Anderson MI, Hayman R, Chakraborty S (2004) A proposed architecture for the neural representation of spatial context. Neurosci Biobehav Rev 28:201-218.
20. Knierim JJ, Kudrimoti HS, McNaughton BL (1998) Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J Neurophysiol 80:425-446.
21. Kubie JL (1984) A driveable bundle of microwires for collecting single-unit data from freely moving rats. Physiol Behav 32:115-118.
22. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183-1194.
23. Lee I, Kesner RP (2002) Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nat Neurosci 5:162-168.
24. Lee I, Kesner RP (2003) Differential roles of dorsal hippocampal subregions in spatial working memory with short versus intermediate delay. Behav Neurosci 117:1044-1053.
25. Lee I, Rao G, Knierim JJ (2004a) A double dissociation between hippocampal subfields: differential time time course of CA3 and CA1 place cells for processing changed environments. Neuron 42:803-815.
26. Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004b) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430:456-459.
27. Lenck-Santini PP, Save E, Poucet B (2001) Evidence for a relationship between the firing patterns of hippocampal place cells and rat's performance in a spatial memory task. Hippocampus 11:377-390.
28. Lenck-Santini PP, Rivard B, Muller RU, Poucet B (2005) Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial changes in the environment. Hippocampus 15:356-369.
29. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser MB, Moser EI (2005) Progressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 48:345-358.
30. Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145-156.
31. Markus EJ, Qin YL, Leonard B, 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.
32. Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262:23-81.
33. McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ (1989) Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76:485-496.
34. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199:173-185.
35. Mizumori SJ, McNaughton BL, Barnes CA, Fox KB (1989) Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus. J Neurosci 9:3915-3928.
36. Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951-1968.
37. 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.
38. Muller RU, Stead M, Pach J (1996) The hippocampus as a cognitive graph. J Gen Physiol 107:663-694.
39. Nakazawa K, Sun LD, Quirk MC, Rondi-Reig L, Wilson MA, Tonegawa S (2003) Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38:305-315.
40. 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.
41. O'Keefe J, Nadel L (1978) Hippocampus as a cognitive map. Oxford, UK: Clarendon.
42. O'Keefe J, Speakman A (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68:1-27.
43. O'Neill J, Senior TJ, Allen K, Huxter JR, Csicsvari J (2008) Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci 11:209-215.
44. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, Ed 5. Sydney: Academic.
45. Paz-Villagrán V, Save E, Poucet B (2004) Independent coding of connected environments by place cells. Eur J Neurosci 20:1379-1390.
46. Poucet B (1993) Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. Psychol Rev 100:163-182.
47. Poucet B, Benhamou S (1997) The neuropsychology of spatial cognition in the rat. Crit Rev Neurobiol 11:101-120.
48. Renaudineau S, Poucet B, Save E (2007) Flexible use of proximal objects and distal cues by hippocampal place cells. Hippocampus 17:381-395.
49. Rivard B, Li Y, Lenck-Santini PP, Poucet B, Muller RU (2004) Representation of objects in space by two classes of hippocampal pyramidal cell. J Gen Physiol 124:9-25.
50. Rolls ET, Kesner RP (2006) A computational theory of hippocampal function and empirical tests of the theory. Prog Neurobiol 79:1-48.
51. Samsonovich A, McNaughton BL (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900-5920.
52. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.
53. Treves A, Rolls ET (1992) Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2:189-199.
54. Vazdarjanova A, Guzowski JF (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489-6496.
55. Wills TJ, Lever C, Cacucci F, Burgess N, O'Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308:873-876.
56. Witter MP, Amaral DG (2004) Hippocampal formation. In: The rat nervous system, Ed 3 (Paxinos GT, ed), pp 635-704. San Diego: Academic.
57. Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397:613-616.
58. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27:623-633.