Differential functional response in the posteromedial cortices and hippocampus to stimulus repetition during successful memory encoding

Human Brain Mapping

Volumn 34, Issue 7, 2013, Pages 1568-1578

  Vannini, Patrizia ^a,b   Hedden, Trey ^a   Sullivan, Caroline ^a   Sperling, Reisa A ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Episodic memory; Functional MRI; Hippocampus; Posteromedial cortex; Repetition

Indexed keywords

ADULT; ARTICLE; EPISODIC MEMORY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; MALE; MIDDLE TEMPORAL GYRUS; PRIORITY JOURNAL; TASK PERFORMANCE;

ADULT; ASSOCIATION LEARNING; BRAIN MAPPING; CEREBRAL CORTEX; FACE; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; MEMORY; NAMES; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PHOTIC STIMULATION; YOUNG ADULT;

EID: 84879201641     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22011     Document Type: Article

References (74)

1. Addis DR, McIntosh AR, Moscovitch M, Crawley AP, McAndrews MP (2004): Characterizing spatial and temporal features of autobiographical memory retrieval networks: A partial least squares approach. Neuroimage 23: 1460-1471.
2. Addis DR, Wong AT, Schacter DL (2007): Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration. Neuropsychologia 45: 1363-1377.
3. Anderson AK, Christoff K, Panitz D, De Rosa E, Gabrieli JDE (2003): Neural correlates of the automatic processing of threat facial signals. J Neurosci 23: 5627-5633.
4. Buckner R, Petersen S, Ojemann J, Miezin F, Squire L, Raichle M (1995): Functional anatomical studies of explicit and implicit memory retrieval tasks. J Neurosci 15: 12-29.
5. Buckner R, Andrews-Hanna JR, Schacter DL (2008): The brain's default network: Anatomy, function, and relevance to disease. Ann NY Acad Sci 1124: 1-38.
6. Burianova H, McIntosh AR, Grady CL (2010): A common functional brain network for autobiographical, episodic, and semantic memory retrieval. Neuroimage 49: 865-874.
7. Cabeza R, Ciaramelli E, Olson IR, Moscovitch M (2008): The parietal cortex and episodic memory: An attentional account. Nat Rev Neurosci 9: 613-625.
8. Chua EF, Schacter DL, Rand-Giovannetti E, Sperling RA (2007): Evidence for a specific role of the anterior hippocampal region in successful associative encoding. Hippocampus 17: 1071-1080.
9. Daselaar SM, Veltman DJ, Rombouts SARB, Raaijmakers JGW, Jonker C (2003): Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. Brain 126: 43-56.
10. Daselaar SM, Prince SE, Cabeza R (2004): When less means more: Deactivations during encoding that predict subsequent memory. Neuroimage 23: 921-927.
11. Daselaar SM, Prince SE, Dennis NA, Kim H, Cabeza R (2009): Posterior midline and ventral parietal acitivity is associated with retrieval success and encoding failure. Front Hum Neurosci 3: 1-10.
12. Desimone R (1996): Neural mechanisms for visual memory and their role in attention. Proc Natl Acad Sci USA 93: 13494-13499.
13. Eichenbaum H (2000): A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1: 41-50.
14. Fahy FL, Riches IP, Brown MW (1993): Neuronal activity related to visual recognition memory: Long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex. Exp Brain Res 96: 457-472.
15. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004): Automatically Parcellating the Human Cerebral Cortex. Cereb Cortex 14: 11-22.
16. Gilbert SJ, Armbruster DJN, Panagiotidi M (2012): Similarity between brain activity at encoding and retrieval predicts successful realization of delayed intentions. J Cogn Neurosci 24: 93-105.
17. Golby A, Silverberg G, Race E, Gabrieli S, O'Shea J, Knierim K, Stebbins G, Gabrieli J (2005): Memory encoding in Alzheimer's disease: An fMRI study of explicit and implicit memory. Brain 128: 773-787.
18. Gonsalves BD, Kahn I, Curran T, Norman KA, Wagner AD (2005): Memory strength and repetition suppression: multimodal imaging of medial temporal cortical contributions to recognition. Neuron 47: 751-761.
19. Greicius MD, Menon V (2004): Default-mode activity during a passive sensory task: Uncoupled from deactivation but impacting activation. J Cogn Neurosci 16: 1484-1492.
20. Grill-Spector K, Henson R, Martin A (2006): Repetition and the brain: Neural models of stimulus-specific effects. Trend Cogn Sci 10: 14-23.
21. Grön G, Bittner D, Schmitz B, Wunderlich AP, Tomczak R, Riepe MW (2003): Variability in memory performance in aged healthy individuals: An fMRI study. Neurobiol Aging 24: 453-462.
22. Haxby JV, Hoffman EA, Gobbini IM (2000): The distributed human neural system for face perception. Trends Cog Sci 4: 223-233.
23. Henson R, Rugg M (2003): Neural response suppression, haemodynamic repetition effects, and behavioral priming. Neuropsychologia 41: 263-270.
24. Huijbers W, Pennartz CM, Cabeza R, Daselaar SM (2009): When learning and remembering compete: A functional MRI study. PLoS Biol 13: 7:e11.
25. Huijbers W, Pennartz CMA, Cabeza R, Daselaar SM (2011): The hippocampus is coupled with the default network during memory retrieval but not during memory encoding. PLoS ONE 6: e17463.
26. Ishai A, Ungerleider LG, Martin A, Schouten JL, Haxby JV (1999): Distributed representation of objects in the human ventral visual pathway. PNAS 96: 9379-9384.
27. Ishai A, Pessoa L, Bikle PC, Ungerleider LG (2004): Repetition suppression of faces is modulated by emotion. Proc Natl Acad Sci USA 101: 9827-9832.
28. Jaiswal N, Ray W, Slobounov S (2010): Encoding of visual-spatial information in working memory requires more cerebral efforts than retrieval: Evidence from an EEG and virtual reality study. Brain Res 1347: 80-89.
29. Johnson SC, Baxter LC, Susskind-Wilder L, Conngor DJ, Sabbagh MN, Caselli RJ (2004): Hippocampal adaptation to face repetition in healthy elderly and mild cognitive impairment. Neuropsychologia 42: 980-989.
30. Johnson MK, Raye CL, Mitchell KJ, Touryan SR, Greene EJ, Nolen-Hoeksema S (2006): Dissociating medial frontal and posterior cingulate activity during self-reflection. Soc Cogn Affect Neurosci 1: 56-64.
31. Johnson JD, Muftuler LT, Rugg MD (2008a): Multiple repetitions reveal functionally and anatomically distinct patterns of hippocampal activity during continuous recognition memory. Hippocampus 18: 975-980.
32. Johnson SC, Schmitz TW, Asthana S, Gluck MA, Myers C (2008b): Associative learning over trials activates the hippocampus in healthy elderly but not mild cognitive impairment. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 15: 129-145.
33. Johnson MK, Nolen-Hoeksema S, Mitchell KJ, Levin Y (2009): Medial cortex activity, self-reflection and depression. Soc Cogn Affect Neurosci 4: 313-327.
34. Kanwisher N, McDermott J, Chun MM (1997): The fusiform face area: A module in human extrastriate cortex specialized for face perception. J Neurosci 17: 4302-4311.
35. Kao Y-C, Davis ES, Gabrieli JDE (2005): Neural correlates of actual and predicted memory formation. Nat Neurosci 8: 1776-1783.
36. Kim H, Daselaar SM, Cabeza R (2009): Overlapping brain activity between episodic memory encoding and retrieval: Roles of the task positive and task negative networks. Neuroimage 49: 1045-1054.
37. Koutstaal W, Wagner AD, Rotte M, Maril A, Buckner RL, Schacter DL (2001): Perceptual specificity in visual object priming: Functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex. Neuropsychologia 39: 184-199.
38. Mangels JA, Manzi A, Summerfield C (2009): The first does the work, but the third time's the charm: The effects of massed repetition on episodic encoding of multimodal face-name associations. J Cogn Neurosci 22: 457-473.
39. Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN (2007): Wandering minds: The default network and stimulus-independent thought. Science 315: 393-395.
40. Mazoyer B, Zago L, Mellet E, Bricogne S, Etard O, Houde O, Crivello F, Joliot M, Petit L, Tzourio-Mazoyer N (2001): Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res Bull 54: 287-298.
41. McKiernan KA, Kaufman JN, Kucera-Thompson J, Binder JR (2003): A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. J Cogn Neurosci 15: 394-408.
42. McKiernan KA, D'Angelo BR, Kaufman JN, Binder JR (2006): Interrupting the "stream of consciousness": An fMRI investigation. Neuroimage 29: 1185-1191.
43. Miller EK, Li L, Desimone R (1991): A neural mechanism for working and recognition memory in inferior temporal cortex. Science 254: 1377-1379.
44. Miller SL, Celone K, DePeau K, Diamond E, Dickerson BC, Rentz D, Pihlajamaki M, Sperling RA (2008): Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation. Proc Natl Acad Sci USA 105: 2181-2186.
45. Orfanidou E, Marslen-Wilson WD, Davis MH (2006): Neural response suppression predicts repetition priming of spoken words, and pseudo words. J Cogn Neurosci 18: 1237-1252.
46. Otten LJ, Rugg MD (2001): When more means less: Neural activity related to unsuccessful memory encoding. Curr Biol 11: 1528-1530.
47. Park DC, Polk TA, Hebrank A, Jenkins LJ (2010): Age differences in default mode activity on easy and difficult spatial judgement tasks. Front Hum Neurosci 3: 1-12.
48. Persson J, Lustig C, Nelson JK, Reuter-Lorenz PA (2007): Age differences in deactivation: A link to cognitive control? J Cogn Neurosci 19: 1021-1032.
49. Pihlajamäki M, DePeau K, Blacker D, Sperling RA (2008): Impaired medial temporal repetition suppression is related to failure of parietal deactivation in Alzheimer disease. Am J Geriatr Psychiatry 16: 283-291.
50. Pihlajamäki M, O'Keefe K, Bertram L, Tanzi RE, Dickerson BD, Blacker D, Albert MS, Sperling RA (2009): Evidence of altered posteromedial cortical fMRI activity in subjects at risk for Alzheimer disease. Alzheimer Dis Assoc Disord 24: 28-36.
51. Puce A, Allison T, McCarthy G (1999): Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. Cereb Cortex 9: 445-458.
52. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001): A default mode of brain function. Proc Natl Acad Sci USA 98: 676-682.
53. Rand-Giovannetti E, Chua EF, Driscoll AE, Schacter DL, Albert MS, Sperling RA (2006): Hippocampal and neocortical activation during repetitive encoding in older adults. Neurobiol Aging 27: 173-182.
54. Riches IP, Wilson FA, Brown MW (1991): The effects of visual stimulation and memory on the neurons of the hippocampal formation and the neighboring parahippocampal gyurs and the inferior temporal cortex of teh primate. J Neurosci 11: 1763-1779.
55. Rugg MD, Otten LJ, Henson RNA (2002): The neural basis of episodic memory: Evidence from functional neuroimaging. Philos Trans R Soc B 357: 1097-1110.
56. Schacter DL, Buckner RL (1998): Priming and the brain. Neuron 20: 185-195.
57. Shannon BJ, Buckner RL (2004): Functional-anatomic correlates of memory retrieval that suggest nontraditional processing roles for multiple distinct regions within posterior parietal cortex. J Neurosci 24: 10084-10092.
58. Shrager Y, Kirwan CB, Squire LR (2008): Activation in both hippocampus and perirhinal cortex predicts the memory strenght of subsequently remembered information. Neuron 59: 547-553.
59. Shulman GL, Fiez JA, Corbetta M, Buckner RL, Miezin FM, Raichle ME, Petersen SE (1997): Common blood flow changes across visual tasks: II. decreases in cerebral cortex. J Cogn Neurosci 9: 648-663.
60. Simons JS, Koutstaal W, Prince S, Wagner AD, Schacter DL (2003): Neural mechanisms of visual object priming: Evidence for perceptual and semantic distinctions in fusiform cortex. Neuroimage 19: 613-626.
61. Soldan A, Gazes Y, Hilton HJ, Stern Y (2008): Aging does not affect brain patterns of repetition effects associated with perceptual priming of novel objects. J Cogn Neurosci 20: 1762-1776.
62. Spaniol J, Davidson PSR, Kim ASN, Han H, Moscovitch M, Grady CL (2009): Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation. Neuropsychologia 47: 1765-1779.
63. Sperling R, Chua E, Cocchiarella A, Rand-Giovannetti E, Poldrack R, Schacter DL, Albert M (2003a): Putting names to faces: Successful encoding of associative memories activates the anterior hippocampal formation. Neuroimage 20: 1400-1410.
64. Sperling RA, Bates JF, Chua EF, Cocchiarella AJ, Rentz DM, Rosen BR, Schacter DL, Albert MS (2003b): fMRI studies of associative encoding in young and elderly controls and mild Alzheimer's disease. J Neurol Neurosurg Psychiatry 74: 44-50.
65. Sperling RA, LaViolette PS, O'Keefe K, O'Brien J, Rentz DM, Pihlajamaki M, Marshall G, Hyman BT, Selkoe DJ, Hedden T, Buckner RL, Becker JA, Johnson KA (2009): Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63: 178-188.
66. Suzuki M, Johnson JD, Rugg MD (2010): Decrements in hippocampal activity with item repetition during continuous recognition: An fMRI study. J Cogn Neurosci 1-11.
67. Svoboda E, McKinnon MC, Levine B (2006): The functional neuroanatomy of autobiographical memory: A meta-analysis. Neuropsychologia 44: 2189-2208.
68. Talairach J, Tournoux P (1988): Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme Medical Publishers.
69. Tulving E, Kroll NEA (1995): Novelty assessment in the brain and long-term memory encoding. Psychonomic Bull Rev 2: 387-390.
70. Uncapher MR, Wagner AD (2009): Posterior parietal cortex and episodic encoding: Insights from fMRI subsequent memory effects and dual-attention theory. Neurobiol Learn Mem 91: 139-154.
71. Vannini P, O'Brien J, O'Keefe K, Pihlajamaki M, LaViolette PS, Sperling RA (2011): What goes down must come up: Role of the posteromedial cortices in encoding and retrieval. Cereb Cortex 21: 22-34.
72. Wagner AD, Davachi L (2001): Cognitive neuroscience: Forgetting of things past. Curr Biol 11: R964-R967.
73. Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998): Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18: 411-418.
74. Wiggs CL, Martin A (1998): Properties and mechanisms of perceptual priming. Curr Opin Neurobiol 8: 227-233.