A Working Memory Buffer in Parahippocampal Regions: Evidence from a Load Effect during the Delay Period

Cerebral Cortex

Volumn 26, Issue 5, 2016, Pages 1965-1974

  Schon, Karin ^a,b,c   Newmark, Randall E ^a,c   Ross, Robert S ^a,c   Stern, Chantal E ^a,c  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

encoding; high resolution fMRI; hippocampus; maintenance; matching to sample

Indexed keywords

ADULT; ARTICLE; ENTORHINAL CORTEX; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HUMAN; HUMAN EXPERIMENT; MALE; MEDIAL TEMPORAL LOBE; NORMAL HUMAN; PARAHIPPOCAMPAL GYRUS; PERIRHINAL CORTEX; PRIORITY JOURNAL; SUBICULUM; TASK PERFORMANCE; WORKING MEMORY; BRAIN MAPPING; DECISION MAKING; HIPPOCAMPUS; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; SHORT TERM MEMORY; TEMPORAL LOBE; YOUNG ADULT;

ADULT; BRAIN MAPPING; CHOICE BEHAVIOR; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; NEURAL PATHWAYS; PARAHIPPOCAMPAL GYRUS; PHOTIC STIMULATION; TEMPORAL LOBE; YOUNG ADULT;

EID: 84965182996     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv013     Document Type: Article

References (83)

1. Awipi T, Davachi L. 2008. Content-specific source encoding in human medial temporal lobe. J Exp Psychol Learn Mem Cogn. 34:769-779.
2. Axmacher N, Haupt S, Cohen MX, Elger CE, Fell J. 2009. Interference of working memory load with long-term memory formation. Eur J Neurosci. 29:1501-1513.
3. Axmacher N, Mormann F, Fernández G, Cohen MX, Elger CE, Fell J. 2007. Sustained neural activity patterns during working memory in the human medial temporal lobe. J Neurosci. 27:7807-7816.
4. Axmacher N, Schmitz DP, Weinreich I, Elger CE, Fell J. 2008. Interaction of working memory and long-term memory in the medial temporal lobe. Cereb Cortex. 18:2868-2878.
5. Braver T, Cohen J, Nystrom L, Jonides J, Smith E, Noll D. 1997. A parametric study of prefrontal cortex involvement in human working memory. Neuroimage. 5:49-62.
6. Cairo TA, Liddle PF, Woodward TS, Ngan ETC. 2004. The influence of working memory load on phase specific patterns of cortical activity. Brain Res Cogn Brain Res. 21:377-387.
7. Carr VA, Engel SA, Knowlton BJ. 2013. Top-down modulation of hippocampal encoding activity as measured by high-resolution functional MRI. Neuropsychologia. 51:1829-1837.
8. Diana RA, Yonelinas AP, Ranganath C. 2008. High-resolution multi-voxel pattern analysis of category selectivity in the medial temporal lobes. Hippocampus. 18:536-541.
9. Diana RA, Yonelinas AP, Ranganath C. 2007. Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn Sci. 11:379-386.
10. Druzgal TJ, D'Esposito M. 2003. Dissecting contributions of prefrontal cortex and fusiform face area to face working memory. J Cogn Neurosci. 15:771-784.
11. Duncan K, Ketz N, Inati SJ, Davachi L. 2012. Evidence for area CA1 as a match/mismatch detector: a high-resolution fMRI study of the human hippocampus. Hippocampus. 22:389-398.
12. Duvernoy HM. 2005. The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI. 3rd ed. Berlin, Germany: Springer.
13. Egorov A, Hamam B, Fransén E, Hasselmo ME, Alonso AA. 2002. Graded persistent activity in entorhinal cortex neurons. Nature. 420:173-178.
14. Epstein R, Harris A, Stanley D, Kanwisher N. 1999. The parahippocampal place area: recognition, navigation, or encoding? Neuron. 23:115-125.
15. Epstein R, Kanwisher N. 1998. A cortical representation of the local visual environment. Nature. 392:598-601.
16. Epstein RA, Parker WE, Feiler AM. 2007. Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci. 27:6141-6149.
17. Felleman DJ, Van Essen DC. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1:1-47.
18. Fernández G, Brewer JB, Zhao Z, Glover GH, Gabrieli JD. 1999. Level of sustained entorhinal activity at study correlates with subsequent cued-recall performance: a functional magnetic resonance imaging study with high acquisition rate. Hippocampus. 9:35-44.
19. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. 1995. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 33:636-647.
20. Fransén E, Alonso AA, Dickson CT, Magistretti J, Hasselmo ME. 2004. Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus. 14:368-384.
21. Fransén E, Alonso AA, Hasselmo ME. 2002. Simulations of the role of the muscarinic-activated calcium-sensitive nonspecific cation current INCM in entorhinal neuronal activity during delayed matching tasks. J Neurosci. 22:1081-1097.
22. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, Kiefer B, Haase A. 2002. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med. 47:1202-1210.
23. Hannula DE, Ranganath C. 2008. Medial temporal lobe activity predicts successful relational memory binding. J Neurosci. 28:116-124.
24. Hasselmo ME, Stern CE. 2006. Mechanisms underlying working memory for novel information. Trends Cogn Sci. 10:487-493.
25. Insausti R, Amaral DG, Cowan WM. 1987. The entorhinal cortex of the monkey: II. Cortical afferents. J Comp Neurol. 264:356-395.
26. Insausti R, Juottonen K, Soininen H, Insausti AM, Partanen K, Vainio P, Laakso MP, Pitka A. 1998. MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. Am J Neuroradiol. 19:659-671.
27. Jeneson A, Mauldin KN, Squire LR. 2010. Intact working memory for relational information after medial temporal lobe damage. J Neurosci. 30:13624-13629.
28. Jensen O, Lisman JE. 2005. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci. 28:67-72.
29. Jensen O, Lisman JE. 1996. Novel lists of 7 +/- 2 known items can be reliably stored in an oscillatory short-term memory network: interaction with long-term memory. Learn Mem. 3:257-263.
30. Jensen O, Lisman JE. 1998. An oscillatory short-term memory buffer model can account for data on the Sternberg task. J Neurosci. 18:10688-10699.
31. Jha A, McCarthy G. 2000. The influence of memory load upon delay-interval activity in a working-memory task: an event-related functional MRI study. J Cogn Neurosci. 12:90-105.
32. Jochems A, Yoshida M. 2013. Persistent firing supported by an intrinsic cellular mechanism in hippocampal CA3 pyramidal cells. Eur J Neurosci. 38:2250-2259.
33. Kirwan CB, Jones CK, Miller MI, Stark CEL. 2007. High-resolution fMRI investigation of the medial temporal lobe. Hum Brain Mapp. 28:959-966.
34. Kirwan CB, Stark CEL. 2007. Overcoming interference: an fMRI investigation of pattern separation in the medial temporal lobe. Learn Mem. 14:959-966.
35. Klink R, Alonso A. 1997. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol. 77:1829-1843.
36. Knauer B, Jochems A, Valero-Aracama MJ, Yoshida M. 2013. Longlasting intrinsic persistent firing in rat CA1 pyramidal cells: a possible mechanism for active maintenance of memory. Hippocampus. 23:820-831.
37. Kochan NA, Valenzuela M, Slavin MJ, McCraw S, Sachdev PS, Breakspear M. 2011. Impact of load-related neural processes on feature binding in visuospatial working memory. PLoS One. 6:e23960.
38. Koene RA, Gorchetchnikov A, Cannon RC, Hasselmo ME. 2003. Modeling goal-directed spatial navigation in the rat based on physiological data from the hippocampal formation. Neural Netw. 16:577-584.
39. Koene RA, Hasselmo ME. 2007. First-in-first-out item replacement in a model of short-term memory based on persistent spiking. Cereb Cortex. 17:1766-1781.
40. Kumaran D, Maguire EA. 2007. Match mismatch processes underlie human hippocampal responses to associative novelty. J Neurosci. 27:8517-8524.
41. Langston RF, Stevenson CH, Wilson CL, Saunders I, Wood ER. 2010. The role of hippocampal subregions in memory for stimulus associations. Behav Brain Res. 215:275-291.
42. Lee ACH, Rudebeck SR. 2010. Investigating the interaction between spatial perception and working memory in the human medial temporal lobe. J Cogn Neurosci. 22:2823-2835.
43. Libby LA, Hannula DE, Ranganath C. 2014. Medial temporal lobe coding of item and spatial information during relational binding in working memory. J Neurosci. 34:14233-14242.
44. Lisman J, Idiart M. 1995. Storage of 7+/-2 short-term memories in oscillatory subcycles. Science. 267:1512-1515.
45. Mainy N, Kahane P, Minotti L, Hoffmann D, Bertrand O, Lachaux J-P. 2007. Neural correlates of consolidation in working memory. Hum Brain Mapp. 28:183-193.
46. McGaughy J, Koene RA, Eichenbaum H, Hasselmo ME. 2005. Cholinergic deafferentation of the entorhinal cortex in rats impairs encoding of novel but not familiar stimuli in a delayed nonmatch-to-sample task. J Neurosci. 25:10273-10281.
47. Miller MI, Beg MF, Ceritoglu C, Stark C. 2005. Increasing the power of functional maps of the medial temporal lobe by using large deformation diffeomorphic metric mapping. Proc Natl Acad Sci USA. 102:9685-9690.
48. Navaroli VL, Zhao Y, Boguszewski P, Brown TH. 2012. Muscarinic receptor activation enables persistent firing in pyramidal neurons from superficial layers of dorsal perirhinal cortex. Hippocampus. 22:1392-1404.
49. Newmark RE, Schon K, Ross RS, Stern CE. 2013. Contributions of the hippocampal subfields and entorhinal cortex to disambiguation during working memory. Hippocampus. 23:467-475.
50. Nichols EA, Kao Y-C, Verfaellie M, Gabrieli JD. 2006. Working memory and long-term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus. 16:604-616.
51. O'Reilly RC, McClelland JL. 1994. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus. 4:661-682.
52. Olsen RK, Nichols EA, Chen J, Hunt JF, Glover GH, Gabrieli JDE, Wagner AD. 2009. Performance-related sustained and anticipatory activity in human medial temporal lobe during delayed match-to-sample. J Neurosci. 29:11880-11890.
53. Pessoa L, Gutierrez E, Bandettini PA, Ungerleider LG. 2002. Neural correlates of visual working memory: fMRI amplitude predicts task performance. Neuron. 35:975-987.
54. Piekema C, Kessels RPC, Mars RB, Petersson KM, Fernández G. 2006. The right hippocampus participates in short-term memory maintenance of object-location associations. Neuroimage. 33:374-382.
55. Preston AR, Bornstein AM, Hutchinson JB, Gaare ME, Glover GH, Wagner AD. 2010. High-resolution fMRI of content-sensitive subsequent memory responses in human medial temporal lobe. J Cogn Neurosci. 22:156-173.
56. Pruessner JC, Köhler S, Crane J, Pruessner M, Lord C, Byrne A, Kabani N, Collins DL, Evans AC. 2002. Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. Cereb Cortex. 12:1342-1353.
57. Pruessner JC, Li LM, Serles W, Pruessner M, Collins DL, Kabani N, Lupien S, Evans AC. 2000. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cereb Cortex. 10:433-442.
58. Ranganath C, Cohen MX, Brozinsky CJ. 2005. Working memory maintenance contributes to long-term memory formation: neural and behavioral evidence. J Cogn Neurosci. 17:994-1010.
59. Ranganath C, D'Esposito M. 2005. Directing the mind's eye: prefrontal, inferior and medial temporal mechanisms for visual working memory. Curr Opin Neurobiol. 15:175-182.
60. Ranganath C, DeGutis J, D'Esposito M. 2004. Category-specific modulation of inferior temporal activity during working memory encoding and maintenance. Brain Res Cogn Brain Res. 20:37-45.
61. Ranganath C, Esposito MD. 2001. Medial temporal lobe activity associated with active maintenance of novel information. Neuron. 31:865-873.
62. Rissman J, Gazzaley A, D'Esposito M. 2008. Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. Cereb Cortex. 18:1618-1629.
63. Ryan J, Cohen NJ. 2004. Processing and short-term retention of relational information in amnesia. Neuropsychologia. 42:497-511.
64. Rypma B, Prabhakaran V, Desmond J, Glover GH, Gabrieli JD. 1999. Load-dependent roles of frontal brain regions in the maintenance of working memory. Neuroimage. 9:216-226.
65. Sakai K, Passingham RE. 2003. Prefrontal interactions reflect future task operations. Nat Neurosci. 6:75-81.
66. Schon K, Hasselmo ME, LoPresti ML, Tricarico MD, Stern CE. 2004. Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: a functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task. J Neurosci. 24:11088-11097.
67. Schon K, Quiroz YT, Hasselmo ME, Stern CE. 2009. Greater working memory load results in greater medial temporal activity at retrieval. Cereb Cortex. 19:2561-2571.
68. Schon K, Ross RS, Hasselmo ME, Stern CE. 2013. Complementary roles of medial temporal lobes and mid-dorsolateral prefrontal cortex for working memory for novel and familiar trial-unique visual stimuli. Eur J Neurosci. 37:668-678.
69. Shrager Y, Levy DA, Hopkins RO, Squire LR. 2008. Working memory and the organization of brain systems. J Neurosci. 28:4818-4822.
70. Staresina BP, Duncan KD, Davachi L. 2011. Perirhinal and parahippocampal cortices differentially contribute to later recollection of object- and scene-related event details. J Neurosci. 31:8739-8747.
71. Stark CEL, Okado Y. 2003. Making memories without trying: medial temporal lobe activity associated with incidental memory formation during recognition. J Neurosci. 23:6748-6753.
72. Sternberg S. 1966. High-speed scanning in human memory. Science. 153:652-654.
73. Suzuki WA, Amaral DG. 1994. Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J Neurosci. 14:1856-1877.
74. Suzuki WA, Miller EK, Desimone R. 1997. Object and place memory in the macaque entorhinal cortex. J Neurophysiol. 78:1062-1081.
75. Tahvildari B, Fransén E, Alonso AA, Hasselmo ME. 2007. Switching between "On " and "Off" states of persistent activity in lateral entorhinal layer III neurons. Hippocampus. 17:257-263.
76. Van Hoesen GW, Pandya DN. 1975a. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res. 95:1-24.
77. Van Hoesen GW, Pandya DN. 1975b. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. efferent connections. Brain Res. 95:39-59.
78. Van Vugt MK, Schulze-Bonhage A, Litt B, Brandt A, Kahana MJ. 2010. Hippocampal gamma oscillations increase with memory load. J Neurosci. 30:2694-2699.
79. Witter M, Van Hoesen GW, Amaral DG. 1989. Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J Neurosci. 9:216-228.
80. Yassa MA, Stark CEL. 2009. A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe. Neuroimage. 44:319-327.
81. Yoshida M, Fransén E, Hasselmo ME. 2008. mGluR-dependent persistent firing in entorhinal cortex layer III neurons. Eur J Neurosci. 28:1116-1126.
82. Young BJ, Otto T, Fox GD, Eichenbaum H. 1997. Memory representation within the parahippocampal region. J Neurosci. 17:5183-5195.
83. Zarahn E, Rakitin B, Abela D, Flynn J, Stern Y. 2005. Positive evidence against human hippocampal involvement in working memory maintenance of familiar stimuli. Cereb Cortex. 15:303-316.