Level of sustained entorhinal activity at study correlates with subsequent cued-recall performance: A functional magnetic resonance imaging study with high acquisition rate

Hippocampus

Volumn 9, Issue 1, 1999, Pages 35-44

  Fernández, Guillén ^a,b,c,d   Brewer, James B ^a   Zhao, Zuo ^a   Glover, Gary H ^a   Gabrieli, John D E ^a  

^a STANFORD UNIVERSITY   (United States)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d Klinik fur Epileptologie   (Germany)

Author keywords

Declarative memory; Encoding; Functional neuroimaging; Human; Medial temporal lobe

Indexed keywords

ADULT; ARTICLE; ELECTROENCEPHALOGRAM; ENTORHINAL CORTEX; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; MEMORY; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; RECALL; TASK PERFORMANCE; TEMPORAL LOBE;

ADULT; BRAIN MAPPING; CUES; ENTORHINAL CORTEX; FEMALE; FUNCTIONAL LATERALITY; HEMODYNAMIC PROCESSES; HUMANS; LANGUAGE; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; MEMORY, SHORT-TERM; MOTOR CORTEX; PREFRONTAL CORTEX; TEMPORAL LOBE; TIME FACTORS;

EID: 0032990448     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1063(1999)9:1<35::AID-HIPO4>3.0.CO;2-Z     Document Type: Article

References (80)

1. Abe K, Inokawa M, Kashiwagi A, Yanagihara T. 1998. Amnesia after a discrete forebrain lesion. J Neurol Neurosurg Psychiatry 65:126-130.
2. Albuquerque EX, Alkondon M, Pereira EFR, Castro NG, Schrattenholz A, Barbosa CTF, Bonfante-Cabarcas R, Arcava Y, Eisenberg HM, Maelicke A. 1997. Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J Pharmacol Exp Ther 280:1117-1136.
3. Alkire MT, Haier RJ, Fallen JH, Cahill L. 1998. Hippocampal, but not amygdala, activity at encoding correlates with long-term, free recall of nonemotional information. Proc Natl Acad Sci USA 95:14506-14510.
4. Amaral DG, Insausti R. 1990. Hippocampal formation. In: Paxinos G, editor. The human nervous system. San Diego: Academic Press. p. 711-755.
5. Awh E, Jonides J, Smith EE, Schumacher EH, Koeppe RA, Katz S. 1996. Dissociation of storage and rehearsal in verbal working memory: evidence from Positron emission tomography. Psychol Sci 7:25-31.
6. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR. 1995. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269:1115-1118.
7. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. 1995. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
8. Bodis-Wollner I, Bucher SF, Seelos KC, Paulus W, Reiser M, Oertel WH. 1997. Functional MRI mapping of occipital and frontal cortical activity during voluntary and imagined saccades. Neurology 49:416-420.
9. Brewer JB, Zhao Z, Desmond JE, Glover GH, Gabrieli JDE. 1998. Making memories: brain activity that predicts how well visual experience will be remembered. Science 281:1185-1187.
10. Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL. 1995. The Amygdala and emotional memory. Nature 377:295-296.
11. Cahill L, Haier RJ, Fallon J, Alkire MT, Tang C, Keator D, Wu J, McGaugh JL. 1996. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc Natl Acad Sci USA 93:8016-8021.
12. De Lacalle S, Lim C, Sobreviela T, Mufson EJ, Hersh LB, Saper CB. 1994. Cholinergic innervation in the human hippocampal formation including the entorhinal cortex. J Comp Neurol 345:321-344.
13. De Lacoste MC, White CL. 1993. The role of cortical connectivity in Alzheimer's disease pathogenesis: A review and a model system. Neurobiol Aging 14:1-16.
14. Démonet JF, Chollet F, Ramsay S, Cardebat D, Nespoulous JL, Wise R, Rascol A, Frackowiak RSJ. 1992. The anatomy of phonological and semantic processing in normal subjects. Brain 115:1753-1768.
15. Dickson CT, Alonso A. 1997. Muscarinic induction of synchronous population activity in the entorhinal cortex. J Neurosci 17:6729-6744.
16. Dolan RJ, Fletcher PC. 1997. Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature 388:582-585.
17. Eichenbaum H, OttoT, Cohen NJ. 1994. Two functional components of the hippocampal memory system. Behav Brain Sci 17:449-518.
18. Eichenbaum H, Schoenbaum G, Young B, Bunsey M. 1996. Functional organization of the hippocampal memory system. Proc Natl Acad Sci USA 93:13500-13507.
19. Fehlau BP, Patil MM, Hasselmo ME. 1998. Time course of modulation of evoked synaptic potentials by ACH and GABA in rat hippocampus. Soc Neurosci Abstr 24:1909.
20. Fernández G, Weyerts H, Schrader-Bölsche M, Tendolkar I, Smid HGOM, Tempelmann C, Hinrichs H, Scheich H, Elger CE, Mangun GR, Heinze HJ. 1998. Successful verbal encoding into episodic memory engages the posterior hippocampus: a parametrically analyzed functional magnetic resonance imaging study. J Neurosci 18:1841-1847.
21. Fletcher PC, Frith CD, Grasby PM, Shallice T, Frackowiak RSJ, Dolan RJ. 1995. Brain systems for encoding and retrieval of auditory-verbal memory. Brain 118:401-416.
22. Fox NC, Warrington EK, Seiffer AL, Agnew SK, Rossor MN. 1998. Presymptomatic cognitive deficits in individuals at risk of familial Alzheimer's disease: a longitudinal prospective study. Brain 121:1631-1639.
23. Frith CD, Friston KJ, Liddle PF, Frackowiak RSJ. 1991. Willed action and the prefrontal cortex in man: a study with PET. Proc R Soc Lond [Biol] 244:241-246.
24. Gabrieli JDE, Desmond JE, Demb JB, Wagner AD, Stone MV, Vaidya CJ, Glover GH. 1996. Functional magnetic resonance imaging of semantic memory processes in the frontal lobes. Psychol Sci 7:278-283.
25. Gabrieli JD, Brewer JB, Desmond JE, Glover GH. 1997. Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276:264-266.
26. Glover GH, Lai S. 1998. Self-navigated spiral fMRI: interleaved versus single-shot. Mag Reson Med 39:361-368.
27. Gomez-Isla T, Price JL, McKeel DW, Morris JC, Growdon JH, Hyman BT. 1996. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16:4491-4500.
28. Grady CL, McIntosh AR, Horwitz B, Maisog JM, Ungerleider LG, Mentis MJ, Pietrini P, Shapiro MB, Haxby JV. 1995. Age-related reductions in human recognition memory due to impaired encoding. Science 269:218-221.
29. Grasby PM, Frith CD, Friston KJ, Frackowiak RSJ, Dolan RJ. 1993. Activation of the human hippocampal formation during auditory-verbal long-term memory function. Neurosci Lett 163:185-188.
30. Hasselmo ME, Wyble P, Wallenstein GV. 1996. Encoding and retrieval of episodic memories: role of cholinergic and GAB Aergic modulation in the hippocampus. Hippocampus 6:693-708.
31. Hasselmo ME, Linster C. Neuromodulation and memory formation. In: Katz PS editor. Beyond neurotransmission: the role of neuromodulation in information flow and neuronal circuit flexibility. Oxford: Oxford University Press. in press.
32. Haxby JV, Ungerleider LG, Horwitz B, Maisog JM, Rapoport SI, Grady CL. 1996. Face encoding and recognition in the human brain. Proc Natl Acad Sci USA 93:922-927.
33. Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL. 1984. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225:1168-1170.
34. Insausti R, Amaral DG, Cowan WM. 1987. The entorhinal cortex of the monkey: II. cortical afférents. J Comp Neurol 264:356-395.
35. Insausti R, Juottonen K, Insausti AM, Partanen K, Vainio P, Laasko MP, Pitkänen A. 1998. MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. Am J Neuroradiol 19:659-671.
36. Jackson GD, Duncan JS. 1996. MRI neuroanatomy: a new angle on the brain. New York: Churchill Livingstone.
37. Juottonen K, Lehtovirta M, Helisalmi S, Riekkinen PJ, Soininen H. 1998. Major decrease in the volume of the entorhinal cortex in patients with Alzheimer's disease carrying the apolipoprotein E epsilon4 allele. J Neurol Neurosurg Psychiatry 65:322-327.
38. Kapur S, Craik FIM, Tulving E, Wilson AA, Houle S, Brown GM. 1994. Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. Proc Natl Acad Sci USA 91:2008-2011.
39. Kato T, Erhard P, Takayama Y, Strupp J, Le TH, Ogawa S, Ugurbil K 1998. Human hippocampal long-term sustained response during word memory processing. Neuroreport 20:1041-1047.
40. Kelley WM, Miezin FM, McDermott KB, Buckner RL, Raichle ME, Cohen NJ, Ollinger JM, Akbudak E, Conturo TE, Snyder AZ, Peterson SE. 1998. Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron 20:927-936.
41. Kucera H, Erancis WN. 1967. Computational analysis of present day american english. Providence: Brown University Press.
42. La Rue A. 1992. Aging and neuropsychological assessment. New York: Plenum Press.
43. Leonard BW, Amaral DG, Squire LR, Zola-Morgan S. 1995. Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex. J Neurosci 15:5637-5659.
44. Lepage M, Habib R, Tulving E. 1998. Hippocampal PET activations of memory encoding and retrieval: The HIPER model. Hippocampus 8:313-322.
45. Lewis PR, Shute CCD. 1967. The cholinergic limbic system: Projections to hippocampal formation, medial cortex, nuclei of ascending cholinergic reticular system, and the subfornical organ and supraoptic crest. Brain 90:521-540.
46. McCormick DA. 1990. Cellular mechanisms of cholinergic control of neocortical and thalamic neuronal excitability. In: Steriade M, Biesold D, editors. Brain cholinergic systems. Oxford: Oxford University Press. p. 236-264.
47. Mesulam MM, Hersh LB, Mash DC, Gelua C. 1992. Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: a choline acetyltransferase study. J Comp Neurol 318:316-328.
48. Metherate R, Cox CL, Ashe JH. 1992. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12:4701-4711.
49. Meunier M, Bachevalier J, Mishkin M, Murray EA. 1993. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 13:5418-5432.
50. Meunier M, Hadfield W, Bachevalier J, Murray EA. 1996. Effects of rhinal cortex lesions combined with hippocampectomy on visual recognition memory in rhesus monkeys. J Neurophysiol 75:1190-1205.
51. Mishkin M, Suzuki WA, Gadian DG, Vargha-Khadem F. 1997. Hierarchical organization of cognitive memory. Philos Trans R Soc Lond [Biol] 352:1461-1467.
52. Mishkin M, Vargha-Khadem F, Gadian DG. 1998. Amnesia and the organization of the hippocampal system. Hippocampus 8:212-216.
53. Mizumori SJY, Ward KE, Lavoie AM. 1992. Medial septal modulation of entorhinal single unit activity in anesthetized and freely moving rats. Brain Res 570:188-197.
54. Mrzljak L, Levey AI, Goldman-Rakic PS. 1993. Association of m1 and m2 muscarinic receptor proteins with asymmetric synapses in the primate cerebral cortex: morphological evidence for cholinergic modulation of excitatory neurotransmission. Proc Natl Acad Sci USA 90:5194-5198.
55. Murray EA, Mishkin M. 1986. Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy. J Neurosci 6:1991-2003.
56. Nissen MJ, Knopman DS, Schacter DL. 1987. Neurochemical dissociation of memory systems. Neurology 37:789-794.
57. Palier KA. 1990. Recall and stem-completion have different electrophysiological correlates and are modified differentially by directed forgetting. J Exp Psychol Learn Mem Cogn 16:1021-1032.
58. Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME. 1988. Positron emission tomographic studies of cortical anatomy of single-word processing. Nature 331:585-589.
59. Purdon PL, Weisskoff RM. 1998. Effects of temporal autocorrelation due to physiological noise and stimulus paradigm on voxel-level false-positive rates in fMRI. Hum Brain Mapping 6:239-249.
60. Raichle ME, Fiez JA, Videen TO, MacLeod AMK, Pardo JV, Fox PT, Petersen SE. 1994. Practice-related changes in human brain functional anatomy during nonmotor learning. Cereb Cortex 4:8-26.
61. Ridley RM, Murray TK, Johnson JA, Baker HF. 1986. Learning impairment following lesion of the basal nucleus of Meynert in the marmoset: modification by cholinergic drugs. Brain Res 376:108-116.
62. Rombouts SARB, Machielsen WCM, Witter MP, Barkhof F, Lindeboom J, Scheltens P. 1997. Visual association encoding activates the medial temporal lobe: a functional magnetic resonance imaging study. Hippocampus 7:594-601.
63. Scoville WB, Milner B. 1957. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21.
64. Schacter DL, Wagner AD. 1999. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 9:7-24.
65. Shallice T, Fletcher P, Frith CD, Grasby P, Frackowiak RSJ, Dolan RJ. 1994. Brain regions associated with the acquisation and retrievial of verbal episodic memory. Nature 368:633-635.
66. Siegel S, Castellan NJ. 1988. Nonparametric statistics for the behavioral science, 2nd edition. New York: McGraw-Hill. 1988.
67. Squire LR, Zola-Morgan S. 1991. The medial temporal lobe memory system. Science 253:1380-1386.
68. Stern CE, Corkin S, Gonzalez G, Guimaraes AR, Baker JR, Jennings PJ, Carr CA, Sugiura RM, Vedantham V, Rosen BR. 1996. The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc Natl Acad Sci USA 93:8660-8665.
69. 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.
70. Suzuki WA, Zola-Morgan S, Squire LR, Amaral DG. 1993. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long lasting memory impairment in the visual and tactual modalities. J Neurosci 13:2430-2451.
71. Suzuki WA, Miller EK, Desimone R. 1997. Object and place memory in the macaque entorhinal cortex. J Neurophysiol 78:1062-1081.
72. Tang Y, Mishkin M, Aigner TG. 1997. Effects of muscarinic blockade in perirhinal cortex during visual recognition. Proc Natl Acad Sci USA 94:12667-12669.
73. Tulving E, Markowitsch HJ. 1998. Episodic and declarative memory: role of the hippocampus. Hippocampus 8:198-204.
74. Tulving E, Markowitsch HJ, Kapur S, Habib R, Houle S. 1994. Novelty encoding networks in the human brain: positron emission tomography data. Neuroreport 5:2525-2528.
75. Tulving E, Markowitsch HJ, Craik FIM, Habib R, Houle S. 1996. Novelty and familiarity activations in PET studies of memory encoding and retrieval. Cereb Cortex 6:71-79.
76. Vargha-Khadem F, Gadian DG, Watkins KE, Connelly A, Van Paesschen W, Mishkin M. 1997. Differential Effects of early hippocampal pathology on episodic and semantic memory. Science 277:376-380.
77. Wagner AD, Schacter DL, Rotte M, Koutstaal W, Maril A, Dale AM, Rosen BR, Buckner RL. 1998. Left prefrontal and temporal lobe activation during human encoding is associated with whether experiences are remembered or forgotten. Science 281:1188-1191.
78. Woods RP, Cherry SR, Mazziotta JC. 1992. Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 16:620-633.
79. Young BJ, Otto T, Fox GD, Eichenbaum H. 1997. Memory representation within the parahippocampal region. J Neurosci 17:5183-5195.
80. Zola-Morgan S, Squire LR, Clower RP, Rempel NL. 1993. Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation. J Neurosci 13:251-265.