Perirhinal-Hippocampal Connectivity during Reactivation Is a Marker for Object-Based Memory Consolidation

Neuron

Volumn 79, Issue 6, 2013, Pages 1232-1242

  Vilberg, KaiaL ^a   Davachi, Lila ^b  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; ASSOCIATIVE MEMORY; BEHAVIOR; BOLD SIGNAL; CONNECTOME; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; MALE; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; OBJECT RELATION; PARAHIPPOCAMPAL PLACE AREA; PATTERN RECOGNITION; PERIRHINAL CORTEX; PREDICTION; PRIORITY JOURNAL; TEMPORAL LOBE;

ADOLESCENT; ADULT; ASSOCIATION LEARNING; BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; NEURAL PATHWAYS; OXYGEN; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; REACTION TIME; VOCABULARY; YOUNG ADULT;

EID: 84884281649     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.07.013     Document Type: Article

References (57)

1. Antony J.W., Gobel E.W., O'Hare J.K., Reber P.J., Paller K.A. Cued memory reactivation during sleep influences skill learning. Nat. Neurosci. 2012, 15:1114-1116.
2. Balderas I., Rodriguez-Ortiz C.J., Salgado-Tonda P., Chavez-Hurtado J., McGaugh J.L., Bermudez-Rattoni F. The consolidation of object and context recognition memory involve different regions of the temporal lobe. Learn. Mem. 2008, 15:618-624.
3. Born J., Wilhelm I. System consolidation of memory during sleep. Psychol. Res. 2012, 76:192-203.
4. Brady T.F., Konkle T., Alvarez G.A., Oliva A. Visual long-term memory has a massive storage capacity for object details. Proc. Natl. Acad. Sci. USA 2008, 105:14325-14329.
5. Brown M.W., Aggleton J.P. Recognition memory: what are the roles of the perirhinal cortex and hippocampus?. Nat. Rev. Neurosci. 2001, 2:51-61.
6. Buzsáki G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 1989, 31:551-570.
7. Carr M.F., Karlsson M.P., Frank L.M. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 2012, 75:700-713.
8. Cepeda N.J., Pashler H., Vul E., Wixted J.T., Rohrer D. Distributed practice in verbal recall tasks: A review and quantitative synthesis. Psychol. Bull. 2006, 132:354-380.
9. Cocosco C., Kollokian V., Kwan R.S., Evans A. Brainweb: Online interface to a 3D MRI simulated brain database. Neuroimage 1997, 5:S425.
10. Davachi L. Item, context and relational episodic encoding in humans. Curr. Opin. Neurobiol. 2006, 16:693-700.
11. Davachi L., Mitchell J.P., Wagner A.D. Multiple routes to memory: distinct medial temporal lobe processes build item and source memories. Proc. Natl. Acad. Sci. USA 2003, 100:2157-2162.
12. Diana R.A., Yonelinas A.P., Ranganath C. Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn. Sci. 2007, 11:379-386.
13. Ego-Stengel V., Wilson M.A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 2010, 20:1-10.
14. Eichenbaum H., Yonelinas A.P., Ranganath C. The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 2007, 30:123-152.
15. Friston K.J., Fletcher P.C., Josephs O., Holmes A., Rugg M.D., Turner R. Event-related fMRI: characterizing differential responses. Neuroimage 1998, 7:30-40.
16. Friston K.J., Glaser D.E., Henson R.N., Kiebel S., Phillips C., Ashburner J. Classical and Bayesian inference in neuroimaging: applications. Neuroimage 2002, 16:484-512.
17. Gais S., Albouy G., Boly M., Dang-Vu T.T., Darsaud A., Desseilles M., Rauchs G., Schabus M., Sterpenich V., Vandewalle G., et al. Sleep transforms the cerebral trace of declarative memories. Proc. Natl. Acad. Sci. USA 2007, 104:18778-18783.
18. Jadhav S.P., Kemere C., German P.W., Frank L.M. Awake hippocampal sharp-wave ripples support spatial memory. Science 2012, 336:1454-1458.
19. Ji D., Wilson M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 2007, 10:100-107.
20. Káli S., Dayan P. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat. Neurosci. 2004, 7:286-294.
21. Karlsson M.P., Frank L.M. Awake replay of remote experiences in the hippocampus. Nat. Neurosci. 2009, 12:913-918.
22. Kriegeskorte N., Simmons W.K., Bellgowan P.S.F., Baker C.I. Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 2009, 12:535-540.
23. Larkin A.E., Fahey B., Gobbo O., Callaghan C.K., Cahill E., O'Mara S.M., Kelly A.M. Blockade of NMDA receptors pre-training, but not post-training, impairs object displacement learning in the rat. Brain Res. 2008, 1199:126-132.
24. Lewis P.A., Cairney S., Manning L., Critchley H.D. The impact of overnight consolidation upon memory for emotional and neutral encoding contexts. Neuropsychologia 2011, 49:2619-2629.
25. Litman L., Davachi L. Distributed learning enhances relational memory consolidation. Learn. Mem. 2008, 15:711-716.
26. Marr D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1971, 262:23-81.
27. Milton F., Muhlert N., Butler C.R., Smith A., Benattayallah A., Zeman A.Z. An fMRI study of long-term everyday memory using SenseCam. Memory 2011, 19:733-744.
28. Oliva A., Torralba A. Modeling the shape of the scene: A holistic representation of the spatial envelope. Int. J. Comput. Vis. 2001, 42:145-175.
29. Oudiette D., Antony J.W., Creery J.D., Paller K.A. The role of memory reactivation during wakefulness and sleep in determining which memories endure. J.Neurosci. 2013, 33:6672-6678.
30. Oudiette D., Paller K.A. Upgrading the sleeping brain with targeted memory reactivation. Trends Cogn. Sci. 2013, 17:142-149.
31. Payne J.D., Kensinger E.A. Sleep leads to changes in the emotional memory trace: evidence from FMRI. J.Cogn. Neurosci. 2011, 23:1285-1297.
32. Paz R., Bauer E.P., Paré D. Learning-related facilitation of rhinal interactions by medial prefrontal inputs. J.Neurosci. 2007, 27:6542-6551.
33. Peigneux P., Orban P., Balteau E., Degueldre C., Luxen A., Laureys S., Maquet P. Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol. 2006, 4:e100.
34. Qin Y.L., McNaughton B.L., Skaggs W.E., Barnes C.A. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1997, 352:1525-1533.
35. Ramos J.M. Perirhinal cortex lesions produce retrograde amnesia for spatial information in rats: consolidation or retrieval?. Learn. Mem. 2008, 15:587-596.
36. Ranganath C., Yonelinas A.P., Cohen M.X., Dy C.J., Tom S.M., D'Esposito M. Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia 2004, 42:2-13.
37. Rissman J., Gazzaley A., D'Esposito M. Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage 2004, 23:752-763.
38. Rudoy J.D., Voss J.L., Westerberg C.E., Paller K.A. Strengthening individual memories by reactivating them during sleep. Science 2009, 326:1079.
39. Skaggs W.E., McNaughton B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 1996, 271:1870-1873.
40. Squire L.R., Alvarez P. Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr. Opin. Neurobiol. 1995, 5:169-177.
41. Squire L.R., Wixted J.T., Clark R.E. Recognition memory and the medial temporal lobe: a new perspective. Nat. Rev. Neurosci. 2007, 8:872-883.
42. Staresina B.P., Davachi L. Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding. J.Cogn. Neurosci. 2008, 20:1478-1489.
43. Staresina B.P., Davachi L. Mind the gap: binding experiences across space and time in the human hippocampus. Neuron 2009, 63:267-276.
44. Staresina B.P., Duncan K.D., Davachi L. Perirhinal and parahippocampal cortices differentially contribute to later recollection of object- and scene-related event details. J.Neurosci. 2011, 31:8739-8747.
45. Stark C.E., Squire L.R. When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc. Natl. Acad. Sci. USA 2001, 98:12760-12766.
46. Stickgold R., Hobson J.A., Fosse R., Fosse M. Sleep, learning, and dreams: off-line memory reprocessing. Science 2001, 294:1052-1057.
47. Takashima A., Nieuwenhuis I.L., Jensen O., Talamini L.M., Rijpkema M., Fernández G. Shift from hippocampal to neocortical centered retrieval network with consolidation. J.Neurosci. 2009, 29:10087-10093.
48. Takashima A., Petersson K.M., Rutters F., Tendolkar I., Jensen O., Zwarts M.J., McNaughton B.L., Fernández G. Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc. Natl. Acad. Sci. USA 2006, 103:756-761.
49. Tambini A., Ketz N., Davachi L. Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 2010, 65:280-290.
50. Tubridy S., Davachi L. Medial temporal lobe contributions to episodic sequence encoding. Cereb. Cortex 2011, 21:272-280.
51. van Kesteren M.T., Fernández G., Norris D.G., Hermans E.J. Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proc. Natl. Acad. Sci. USA 2010, 107:7550-7555.
52. Warburton E.C., Koder T., Cho K., Massey P.V., Duguid G., Barker G.R., Aggleton J.P., Bashir Z.I., Brown M.W. Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron 2003, 38:987-996.
53. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
54. Wimber M., Maaß A., Staudigl T., Richardson-Klavehn A., Hanslmayr S. Rapid memory reactivation revealed by oscillatory entrainment. Curr. Biol. 2012, 22:1482-1486.
55. Winters B.D., Bussey T.J. Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J.Neurosci. 2005, 25:52-61.
56. Winters B.D., Bussey T.J. Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. J.Neurosci. 2005, 25:4243-4251.
57. Wixted J.T. The psychology and neuroscience of forgetting. Annu. Rev. Psychol. 2004, 55:235-269.