Can We Reconcile the Declarative Memory and Spatial Navigation Views on Hippocampal Function?

Neuron

Volumn 83, Issue 4, 2014, Pages 764-770

  Eichenbaum, Howard ^a   Cohen, Neal J ^b  

^a BOSTON UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BRAIN MAPPING; BRAIN NERVE CELL; COGNITION; DECLARATIVE MEMORY; EPISODIC MEMORY; HIPPOCAMPUS; HUMAN; INFORMATION PROCESSING; MENTAL FUNCTION; MENTAL PERFORMANCE; NONHUMAN; PRIORITY JOURNAL; RECALL; RECOGNITION; REVIEW; SPATIAL MEMORY; SPATIAL NAVIGATION VIEW; ANIMAL BEHAVIOR; ENTORHINAL CORTEX; EVENT RELATED POTENTIAL; HIPPOCAMPUS POTENTIAL; MEDIAL ENTORHINAL CORTEX; MEMORY CONSOLIDATION; NERVE CELL; NERVE CELL NETWORK; REWARD; SIGNAL DETECTION; SIMULATION; SPATIAL LEARNING; SPATIAL NAVIGATION; TASK PERFORMANCE; ANIMAL; MEMORY; PHYSIOLOGY; SPATIAL ORIENTATION;

ANIMALS; HIPPOCAMPUS; HUMANS; MEMORY; SPATIAL NAVIGATION;

EID: 84907364887     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.07.032     Document Type: Review

References (70)

1. Alyan S., McNaughton B.L. Hippocampectomized rats are capable of homing by path integration. Behav. Neurosci. 1999, 113:19-31.
2. Benhamou S. Path integration by swimming rats. Anim. Behav. 1997, 54:321-327.
3. Berger T.W., Rinaldi P.C., Weisz D.J., Thompson R.F. Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. J.Neurophysiol. 1983, 50:1197-1219.
4. Brandon M.P., Koenig J., Leutgeb J.K., Leutgeb S. New and distinct hippocampal place codes are generated in a new environment during septal inactivation. Neuron 2014, 82:789-796.
5. Bunsey M., Eichenbaum H. Conservation of hippocampal memory function in rats and humans. Nature 1996, 379:255-257.
6. Burgess N., Barry C., O'Keefe J. An oscillatory interference model of grid cell firing. Hippocampus 2007, 17:801-812.
7. Buzsáki G., Moser E.I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 2013, 16:130-138.
8. Cohen N.J., Eichenbaum H. Memory, Amnesia, and the Hippocampal System 1993, MIT Press, Cambridge.
9. Cohen N.J., Squire L.R. Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 1980, 210:207-210.
10. Dudchenko P.A. Why People Get Lost: The Psychology and Neuroscience of Spatial Cognition 2010, Oxford University Press, New York.
11. Duff M.C., Hengst J.A., Tranel D., Cohen N.J. Hippocampal amnesia disrupts verbal play and the creative use of language in social interaction. Aphasiology 2009, 23:926-939.
12. Duff M.C., Kurczek J., Rubin R., Cohen N.J., Tranel D. Hippocampal amnesia disrupts creative thinking. Hippocampus 2013, 23:1143-1149.
13. Dusek J.A., Eichenbaum H. The hippocampus and memory for orderly stimulus relations. Proc. Natl. Acad. Sci. USA 1997, 94:7109-7114.
14. Eacott M.J., Norman G. Integrated memory for object, place, and context in rats: a possible model of episodic-like memory?. J.Neurosci. 2004, 24:1948-1953.
15. Eichenbaum H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 2004, 44:109-120.
16. Eichenbaum H. Memory on time. Trends Cogn. Sci. 2013, 17:81-88.
17. Eichenbaum H., Dudchenko P., Wood E., Shapiro M., Tanila H. The hippocampus, memory, and place cells: is it spatial memory or a memory space?. Neuron 1999, 23:209-226.
18. Etienne A.S., Jeffery K.J. Path integration in mammals. Hippocampus 2004, 14:180-192.
19. Ezzyat Y., Davachi L. Similarity breeds proximity: pattern similarity within and across contexts is related to later mnemonic judgments of temporal proximity. Neuron 2014, 81:1179-1189.
20. Fortin N.J., Wright S.P., Eichenbaum H. Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 2004, 431:188-191.
21. Foster T.C., Castro C.A., McNaughton B.L. Spatial selectivity ofrat hippocampal neurons: dependence on preparedness for movement. Science 1989, 244:1580-1582.
22. Frank L.M., Brown E.N., Wilson M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 2000, 27:169-178.
23. Gothard K.M., Skaggs W.E., Moore K.M., McNaughton B.L. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J.Neurosci. 1996, 16:823-835.
24. Hafting T., Fyhn M., Molden S., Moser M.-B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
25. Hannula D.E., Ranganath C. The eyes have it: hippocampal activity predicts expression of memory in eye movements. Neuron 2009, 63:592-599.
26. Hartley T., Lever C., Burgess N., O'Keefe J. Space in the brain: how the hippocampal formation supports spatial cognition. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369:20120510.
27. Harvey C.D., Coen P., Tank D.W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 2012, 484:62-68.
28. Hasselmo M.E. How We Remember: Brain Mechanisms of Episodic Memory 2012, MIT Press, Cambridge.
29. Hsieh L.T., Gruber M.J., Jenkins L.J., Ranganath C. Hippocampal activity patterns carry information about objects in temporal context. Neuron 2014, 81:1165-1178.
30. Huth J.E. The Lost Art of Finding Our Way 2013, Harvard UniversityPress, Cambridge.
31. Itskov P.M., Vinnik E., Diamond M.E. Hippocampal representation of touch-guided behavior in rats: persistent and independent traces of stimulus and reward location. PLoS ONE 2011, 6:e16462. 10.1371/journal.pone.0016462.
32. Itskov P.M., Vinnik E., Honey C., Schnupp J., Diamond M.E. Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task. J.Neurophysiol. 2012, 107:1822-1834.
33. Kennedy P.J., Shapiro M.L. Motivational states activate distinct hippocampal representations to guide goal-directed behaviors. Proc. Natl. Acad. Sci. USA 2009, 106:10805-10810.
34. Kim S., Sapiurka M., Clark R.E., Squire L.R. Contrasting effects on path integration after hippocampal damage in humans and rats. Proc. Natl. Acad. Sci. USA 2013, 110:4732-4737.
35. Komorowski R.W., Manns J.R., Eichenbaum H. Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J.Neurosci. 2009, 29:9918-9929.
36. Konkel A., Cohen N.J. Relational memory and the hippocampus: representations and methods. Front. Neurosci. 2009, 3:166-174.
37. Konkel A., Warren D.E., Duff M.C., Tranel D.N., Cohen N.J. Hippocampal amnesia impairs all manner of relational memory. Front Hum Neurosci 2008, 2:15.
38. Langston R.F., Wood E.R. Associative recognition and the hippocampus: differential effects of hippocampal lesions on object-place, object-context and object-place-context memory. Hippocampus 2010, 20:1139-1153.
39. MacDonald C.J., Lepage K.Q., Eden U.T., Eichenbaum H. Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 2011, 71:737-749.
40. MacDonald C.J., Carrow S., Place R., Eichenbaum H. Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J.Neurosci. 2013, 33:14607-14616.
41. Maguire E.A., Mullally S.L. The hippocampus: a manifesto for change. J.Exp. Psychol. Gen. 2013, 142:1180-1189.
42. Manns J.R., Howard M.W., Eichenbaum H. Gradual changes in hippocampal activity support remembering the order of events. Neuron 2007, 56:530-540.
43. McKenzie S., Robinson N.T.M., Herrera L., Churchill J.C., Eichenbaum H. Learning causes reorganization of neuronal firing patterns to represent related experiences within a hippocampal schema. J.Neurosci. 2013, 33:10243-10256.
44. McKenzie S., Frank A.J., Kinsky N.R., Porter B., Rivière P.D., Eichenbaum H. Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron 2014, 83:202-215.
45. McNaughton B.L., Barnes C.A., Gerrard J.L., Gothard K., Jung M.W., Knierim J.J., Kudrimoti H., Qin Y., Skaggs W.E., Suster M., Weaver K.L. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J.Exp. Biol. 1996, 199:173-185.
46. McNaughton B.L., Battaglia F.P., Jensen O., Moser E.I., Moser M.-B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 2006, 7:663-678.
47. Milivojevic B., Doeller C.F. Mnemonic networks in the hippocampal formation: from spatial maps to temporal and conceptual codes. J.Exp. Psychol. Gen. 2013, 142:1231-1241.
48. Moita M.A.P., Moisis S., Zhou Y., LeDoux J.E., Blair H.T. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 2003, 37:485-497.
49. Moser E.I., Kropff E., Moser M.-B. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 2008, 31:69-89.
50. Muller R.U., Kubie J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J.Neurosci. 1987, 7:1951-1968.
51. Navratilova Z., McNaughton B.L. Models of path integration in thehippocampal complex. Space, Time and Memory in the Hippocampal Formation 2014, 191-224. Springer-Verlag, Vienna. D. Derdikman, J.J. Knierim (Eds.).
52. Naya Y., Suzuki W.A. Integrating what and when across the primate medial temporal lobe. Science 2011, 333:773-776.
53. Nitz D.A. Spaces within spaces: rat parietal cortex neurons register position across three reference frames. Nat. Neurosci. 2012, 15:1365-1367.
54. O'Keefe J., Burgess N. Geometric determinants of the place fields of hippocampal neurons. Nature 1996, 381:425-428.
55. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press, NewYork.
56. O'Keefe J., Speakman A. Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res. 1987, 68:1-27.
57. Ryan J.D., Althoff R.R., Whitlow S., Cohen N.J. Amnesia is a deficit in relational memory. Psychol. Sci. 2000, 11:454-461.
58. Shapiro M.L., Tanila H., Eichenbaum H. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 1997, 7:624-642.
59. Shapiro M.L., Kennedy P.J., Ferbinteanu J. Representing episodes in the mammalian brain. Curr. Opin. Neurobiol. 2006, 16:701-709.
60. Spiers H.J., Maguire E.A. Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 2006, 31:1826-1840.
61. Teng E., Squire L.R. Memory for places learned long ago is intact after hippocampal damage. Nature 1999, 400:675-677.
62. Tse D., Langston R.F., Kakeyama M., Bethus I., Spooner P.A., Wood E.R., Witter M.P., Morris R.G.M. Schemas and memory consolidation. Science 2007, 316:76-82.
63. Wang J.X., Cohen N.J., Voss J.L. Covert rapid action-memory simulation (CRAMS): A hypothesis of hippocampal-prefrontal interactions for adaptive behavior. Neurobiol. Learn. Mem. 2014, 10.1016/j.nlm.2014.04.003.
64. Watson P.D., Voss J.L., Warren D.E., Tranel D., Cohen N.J. Spatial reconstruction by patients with hippocampal damage is dominated by relational memory errors. Hippocampus 2013, 23:570-580.
65. Whishaw I.Q., Maaswinkel H. Rats with fimbria-fornix lesions are impaired in path integration: a role for the hippocampus in "sense of direction". J.Neurosci. 1998, 18:3050-3058.
66. Wolbers T., Hegarty M. What determines our navigational abilities?. Trends Cogn. Sci. 2010, 14:138-146.
67. Wood E.R., Dudchenko P.A., Eichenbaum H. The global record of memory in hippocampal neuronal activity. Nature 1999, 397:613-616.
68. Wood E.R., Dudchenko P.A., Robitsek R.J., Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000, 27:623-633.
69. Yee L.T., Warren D.E., Voss J.L., Duff M.C., Tranel D., Cohen N.J. The hippocampus uses information just encountered to guide efficient ongoing behavior. Hippocampus 2014, 24:154-164.
70. Zeithamova D., Dominick A.L., Preston A.R. Hippocampal andventral medial prefrontal activation during retrieval-mediated learning supports novel inference. Neuron 2012, 75:168-179.