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Published in: European Radiology 1/2006

01-01-2006 | Neuro

FMRI of working memory in patients with mild cognitive impairment and probable Alzheimer’s disease

Authors: F. Zerrin Yetkin, Roger N. Rosenberg, Myron F. Weiner, Phillip D. Purdy, C. Munro Cullum

Published in: European Radiology | Issue 1/2006

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Abstract

The goals of this study were to evaluate brain activation in patients with probable Alzheimer’s disease (AD), mild cognitive impairment (MCI), and controls while performing a working memory (WM) task. Eleven AD patients, ten MCI subjects, and nine controls underwent functional magnetic resonance imaging (fMRI) while performing a visual WM task. Statistical parametric maps of brain activation were obtained in each group, and group activation difference maps were generated. Ability to perform the task did not differ among the groups. Activation was observed in the parahippocampal region, superior-middle-inferior frontal gyri, parietal region, anterior–posterior cingulate, fusiform gyrus, and basal ganglia. MCI and AD groups showed more activation than the controls in the right superior frontal gyrus, bilateral middle temporal, middle frontal, anterior cingulate, and fusiform gyri. Activation in the right parahippocampal gyrus, left inferior frontal gyrus, bilateral cingulate and lingual gyri, right lentiform nucleus, right fusiform gyrus, and left supramarginal gyrus in the AD group was less than in the MCI group. The WM task evoked activation in widely distributed regions, consistent with previous fMRI studies. AD and MCI patients showed an increased extent of activation and recruitment of additional areas.
Literature
1.
go back to reference McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of the Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology 34:939–944PubMed McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of the Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology 34:939–944PubMed
2.
go back to reference Morris JC, Storandt M, Miller JP, McKeel DW, Price JL, Rubin EH et al (2001) Mild cognitive impairment represents early-stage Alzheimer disease. Arch Neurol 58(3):397–405PubMed Morris JC, Storandt M, Miller JP, McKeel DW, Price JL, Rubin EH et al (2001) Mild cognitive impairment represents early-stage Alzheimer disease. Arch Neurol 58(3):397–405PubMed
3.
go back to reference Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56(3):303–308PubMed Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56(3):303–308PubMed
4.
go back to reference Daly E, Zaitchik D, Copeland M, Schmahmann J, Gunther J, Albert M (2000) Predicting conversion to Alzheimer disease using standardized clinical information. Arch Neurol 57(5):675–680CrossRefPubMed Daly E, Zaitchik D, Copeland M, Schmahmann J, Gunther J, Albert M (2000) Predicting conversion to Alzheimer disease using standardized clinical information. Arch Neurol 57(5):675–680CrossRefPubMed
5.
go back to reference Ernst RL, Hay JW, Fenn C, Tinklenberg J, Yesavage JA (1997) Cognitive function and the costs of Alzheimer disease. An exploratory study. Arch Neurol 54(6):687–693PubMed Ernst RL, Hay JW, Fenn C, Tinklenberg J, Yesavage JA (1997) Cognitive function and the costs of Alzheimer disease. An exploratory study. Arch Neurol 54(6):687–693PubMed
6.
go back to reference Desgranges B, Baron JC, de la Sayette V, Petit-Taboue MC, Benali K, Landeau B et al (1998) The neural substrates of memory systems impairment in Alzheimer’s disease. A PET study of resting brain glucose utilization. Brain 121(Pt 4):611–631PubMed Desgranges B, Baron JC, de la Sayette V, Petit-Taboue MC, Benali K, Landeau B et al (1998) The neural substrates of memory systems impairment in Alzheimer’s disease. A PET study of resting brain glucose utilization. Brain 121(Pt 4):611–631PubMed
7.
go back to reference Killiany RJ, Hyman BT, Gomez-Isla T, Moss MB, Kikinis R, Jolesz F et al (2002) MRI measures of entorhinal cortex vs hippocampus in preclinical AD. Neurology 58(8):1188–1196PubMed Killiany RJ, Hyman BT, Gomez-Isla T, Moss MB, Kikinis R, Jolesz F et al (2002) MRI measures of entorhinal cortex vs hippocampus in preclinical AD. Neurology 58(8):1188–1196PubMed
8.
go back to reference Bookheimer SY, Strojwas MH, Cohen MS et al (2000) Patterns of brain activation in people at risk for Alzheimer’s disease. N Engl J Med 343(7):450–456CrossRefPubMed Bookheimer SY, Strojwas MH, Cohen MS et al (2000) Patterns of brain activation in people at risk for Alzheimer’s disease. N Engl J Med 343(7):450–456CrossRefPubMed
9.
go back to reference Mencl WE, Pugh KR, Shaywitz SE et al (2000) Network analysis of brain activations in working memory: behavior and age relationships. Microsc Res Tech 51(1):64–74CrossRefPubMed Mencl WE, Pugh KR, Shaywitz SE et al (2000) Network analysis of brain activations in working memory: behavior and age relationships. Microsc Res Tech 51(1):64–74CrossRefPubMed
10.
go back to reference Cabeza R, Grady CL, Nyberg L et al (1997) Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J Neurosci 17(1):391–400PubMed Cabeza R, Grady CL, Nyberg L et al (1997) Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J Neurosci 17(1):391–400PubMed
11.
go back to reference Cabeza R, Anderson ND, Houle S, Mangels JA, Nyberg L (2000) Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study. J Cogn Neurosci 12(1):197–206CrossRefPubMed Cabeza R, Anderson ND, Houle S, Mangels JA, Nyberg L (2000) Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study. J Cogn Neurosci 12(1):197–206CrossRefPubMed
12.
go back to reference Grady CL, McIntosh AR, Bookstein F, Horwitz B, Rapoport SI, Haxby JV (1998) Age-related changes in regional cerebral blood flow during working memory for faces. Neuroimage 8(4):409–425CrossRefPubMed Grady CL, McIntosh AR, Bookstein F, Horwitz B, Rapoport SI, Haxby JV (1998) Age-related changes in regional cerebral blood flow during working memory for faces. Neuroimage 8(4):409–425CrossRefPubMed
13.
go back to reference Grady CL, Craik FI (2000) Changes in memory processing with age. Curr Opin Neurobiol 10(2):224–231 Grady CL, Craik FI (2000) Changes in memory processing with age. Curr Opin Neurobiol 10(2):224–231
14.
go back to reference Hazlett EA, Buchsbaum MS, Mohs RC et al (1998) Age-related shift in brain region activity during successful memory performance. Neurobiol Aging 19(5):437–445 Hazlett EA, Buchsbaum MS, Mohs RC et al (1998) Age-related shift in brain region activity during successful memory performance. Neurobiol Aging 19(5):437–445
15.
go back to reference Small SA, Perera GM, DeLaPaz R, Mayeux R, Stern Y (1999) Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer’s disease. Ann Neurol 45(4):466–472CrossRefPubMed Small SA, Perera GM, DeLaPaz R, Mayeux R, Stern Y (1999) Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer’s disease. Ann Neurol 45(4):466–472CrossRefPubMed
16.
go back to reference Rombouts SA, Barkhof F, Veltman DJ et al (2000) Functional MR imaging in Alzheimer’s disease during memory encoding. Am J Neuroradiol 21(10):1869–1875PubMed Rombouts SA, Barkhof F, Veltman DJ et al (2000) Functional MR imaging in Alzheimer’s disease during memory encoding. Am J Neuroradiol 21(10):1869–1875PubMed
17.
go back to reference Kato T, Knopman D, Liu H (2001) Dissociation of regional activation in mild AD during visual encoding: a functional MRI study. Neurology 57(5):812–816PubMed Kato T, Knopman D, Liu H (2001) Dissociation of regional activation in mild AD during visual encoding: a functional MRI study. Neurology 57(5):812–816PubMed
18.
go back to reference Saykin AJ, Flashman LA, Frutiger SA et al (1999) Neuroanatomic substrates of semantic memory impairment in Alzheimer’s disease: patterns of functional MRI activation. J Int Neuropsychol Soc 5(5):377–392CrossRefPubMed Saykin AJ, Flashman LA, Frutiger SA et al (1999) Neuroanatomic substrates of semantic memory impairment in Alzheimer’s disease: patterns of functional MRI activation. J Int Neuropsychol Soc 5(5):377–392CrossRefPubMed
19.
go back to reference Johnson SC, Saykin AJ, Baxter LC et al (2000) The relationship between fMRI activation and cerebral atrophy: comparison of normal aging and alzheimer disease. Neuroimage 11(3):179–187CrossRefPubMed Johnson SC, Saykin AJ, Baxter LC et al (2000) The relationship between fMRI activation and cerebral atrophy: comparison of normal aging and alzheimer disease. Neuroimage 11(3):179–187CrossRefPubMed
20.
go back to reference Thulborn KR, Martin C, Voyvodic JT (2000) Functional MR imaging using a visually guided saccade paradigm for comparing activation patterns in patients with probable Alzheimer’s disease and in cognitively able elderly volunteers. Am J Neuroradiol 21(3):524–531PubMed Thulborn KR, Martin C, Voyvodic JT (2000) Functional MR imaging using a visually guided saccade paradigm for comparing activation patterns in patients with probable Alzheimer’s disease and in cognitively able elderly volunteers. Am J Neuroradiol 21(3):524–531PubMed
21.
go back to reference Burggren AC, Small GW, Sabb FW, Bookheimer SY (2002) Specificity of brain activation patterns in people at genetic risk for Alzheimer disease. Am J Geriatr Psychiatry 10(1):44–51CrossRefPubMed Burggren AC, Small GW, Sabb FW, Bookheimer SY (2002) Specificity of brain activation patterns in people at genetic risk for Alzheimer disease. Am J Geriatr Psychiatry 10(1):44–51CrossRefPubMed
22.
go back to reference Belleville S, Peretz I, Malenfant D (1996) Examination of the working memory components in normal aging and in dementia of the Alzheimer type. Neuropsychologia 34(3):195–207PubMed Belleville S, Peretz I, Malenfant D (1996) Examination of the working memory components in normal aging and in dementia of the Alzheimer type. Neuropsychologia 34(3):195–207PubMed
23.
go back to reference Rochon E, Waters GS, Caplan D (2000) The relationship between measures of working memory and sentence comprehension in patients with Alzheimer’s disease. J Speech Lang Hear Res 43(2):395–413PubMed Rochon E, Waters GS, Caplan D (2000) The relationship between measures of working memory and sentence comprehension in patients with Alzheimer’s disease. J Speech Lang Hear Res 43(2):395–413PubMed
24.
go back to reference Collette F, Van der Linden M, Bechet S, Salmon E (1999) Phonological loop and central executive functioning in Alzheimer’s disease. Neuropsychologia 37(8):905–918PubMed Collette F, Van der Linden M, Bechet S, Salmon E (1999) Phonological loop and central executive functioning in Alzheimer’s disease. Neuropsychologia 37(8):905–918PubMed
25.
go back to reference Baddeley AD, Bressi S, Della Sala S, Logie R, Spinnler H (1991) The decline of working memory in Alzheimer’s disease. A longitudinal study. Brain 114(Pt 6):2521–2542PubMed Baddeley AD, Bressi S, Della Sala S, Logie R, Spinnler H (1991) The decline of working memory in Alzheimer’s disease. A longitudinal study. Brain 114(Pt 6):2521–2542PubMed
26.
go back to reference Smith EE, Jonides J (1998) Neuroimaging analyses of human working memory. Proc Natl Acad Sci U S A 95(20):12061–12068CrossRefPubMed Smith EE, Jonides J (1998) Neuroimaging analyses of human working memory. Proc Natl Acad Sci U S A 95(20):12061–12068CrossRefPubMed
27.
go back to reference Postle BR, Stern CE, Rosen BR, Corkin S (2000) An fMRI investigation of cortical contributions to spatial and nonspatial visual working memory. Neuroimage 11(5 Pt 1):409–423CrossRefPubMed Postle BR, Stern CE, Rosen BR, Corkin S (2000) An fMRI investigation of cortical contributions to spatial and nonspatial visual working memory. Neuroimage 11(5 Pt 1):409–423CrossRefPubMed
28.
go back to reference Smith EE, Geva A, Jonides J, Miller A, Reuter-Lorenz P, Koeppe RA (2001) The neural basis of task-switching in working memory: effects of performance and aging. Proc Natl Acad Sci U S A 98(4):2095–2100CrossRefPubMed Smith EE, Geva A, Jonides J, Miller A, Reuter-Lorenz P, Koeppe RA (2001) The neural basis of task-switching in working memory: effects of performance and aging. Proc Natl Acad Sci U S A 98(4):2095–2100CrossRefPubMed
29.
go back to reference Adler CM, Holland SK, Enseleit S, Strakowski SM (2001) Age-related changes in regional activation during working memory in young adults: an fMRI study. Synapse 42(4):252–257CrossRefPubMed Adler CM, Holland SK, Enseleit S, Strakowski SM (2001) Age-related changes in regional activation during working memory in young adults: an fMRI study. Synapse 42(4):252–257CrossRefPubMed
30.
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed
31.
go back to reference Wechsler D (1987) Wechsler memory scale-revised. Psychological Corporation, San Antonio, Texas Wechsler D (1987) Wechsler memory scale-revised. Psychological Corporation, San Antonio, Texas
32.
go back to reference Delis DC, Kramer JH, Kaplan E, Ober BA (1987) California verbal learning test: adult version. Harcourt Brace, San Antonio, Texas Delis DC, Kramer JH, Kaplan E, Ober BA (1987) California verbal learning test: adult version. Harcourt Brace, San Antonio, Texas
33.
go back to reference Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMed Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMed
34.
go back to reference Hughes CP, Berg L, Danziger WL (1982) A new clinical scale for the staging of dementia. Br J Psychiatry 140:566–572PubMed Hughes CP, Berg L, Danziger WL (1982) A new clinical scale for the staging of dementia. Br J Psychiatry 140:566–572PubMed
35.
go back to reference Hachinski VC, Iliff L, Zilkha E et al (1975) Cerebral blood flow in dementia. Arch Neurol 32:632–637PubMed Hachinski VC, Iliff L, Zilkha E et al (1975) Cerebral blood flow in dementia. Arch Neurol 32:632–637PubMed
36.
go back to reference Beck AT, Ward CH, Mendelson M et al (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571PubMed Beck AT, Ward CH, Mendelson M et al (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571PubMed
37.
go back to reference Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173CrossRefPubMed Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173CrossRefPubMed
38.
go back to reference Cox RW, Hyde JS (1997) Software tools for analysis and visualization of fMRI data. NMR Biomed 10(4–5):171–178CrossRefPubMed Cox RW, Hyde JS (1997) Software tools for analysis and visualization of fMRI data. NMR Biomed 10(4–5):171–178CrossRefPubMed
39.
go back to reference Cox RW, Jesmanowicz A (1999) Real-time 3D image registration for functional MRI. Magn Reson Med 42:1014–1018CrossRefPubMed Cox RW, Jesmanowicz A (1999) Real-time 3D image registration for functional MRI. Magn Reson Med 42:1014–1018CrossRefPubMed
40.
go back to reference Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. In: 3-dimensional proportional system: an approach to cerebral imaging. Thieme Medical Publishers, New York, NY Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. In: 3-dimensional proportional system: an approach to cerebral imaging. Thieme Medical Publishers, New York, NY
41.
go back to reference Studholme C, Cardenas V, Maudsley A, Weiner M (2003) An intensity consistent filtering approach to the analysis of deformation tensor derived maps of brain shape. NeuroImage 19:1638–1649CrossRefPubMed Studholme C, Cardenas V, Maudsley A, Weiner M (2003) An intensity consistent filtering approach to the analysis of deformation tensor derived maps of brain shape. NeuroImage 19:1638–1649CrossRefPubMed
42.
go back to reference Rombouts SA, Barkhof F, Van Meel CS, Scheltens P (2002) Alterations in brain activation during cholinergic enhancement with rivastigmine in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 73(6):665–671CrossRefPubMed Rombouts SA, Barkhof F, Van Meel CS, Scheltens P (2002) Alterations in brain activation during cholinergic enhancement with rivastigmine in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 73(6):665–671CrossRefPubMed
43.
go back to reference Haxby JV, Petit L, Ungerleider LG, Courtney SM (2000) Distinguishing the functional roles of multiple regions in distributed neural systems for visual working memory. Neuroimage 11(5 Pt 1):380–391CrossRefPubMed Haxby JV, Petit L, Ungerleider LG, Courtney SM (2000) Distinguishing the functional roles of multiple regions in distributed neural systems for visual working memory. Neuroimage 11(5 Pt 1):380–391CrossRefPubMed
44.
go back to reference Nystrom LE, Braver TS, Sabb FW, Delgado MR, Noll DC, Cohen JD (2000) Working memory for letters, shapes, and locations: fMRI evidence against stimulus based regional organization in human prefrontal cortex. Neuroimage 11(5 Pt 1):424–446CrossRefPubMed Nystrom LE, Braver TS, Sabb FW, Delgado MR, Noll DC, Cohen JD (2000) Working memory for letters, shapes, and locations: fMRI evidence against stimulus based regional organization in human prefrontal cortex. Neuroimage 11(5 Pt 1):424–446CrossRefPubMed
45.
go back to reference Cabeza R, Dolcos F, Graham R, Nyberg L (2002) Similarities and differences in the neural correlates of episodic memory retrieval and working memory. Neuroimage 16(2):317–330CrossRefPubMed Cabeza R, Dolcos F, Graham R, Nyberg L (2002) Similarities and differences in the neural correlates of episodic memory retrieval and working memory. Neuroimage 16(2):317–330CrossRefPubMed
46.
go back to reference Hautzel H, Mottaghy FM, Schmidt D et al (2002) Topographic segregation and convergence of verbal, object, shape and spatial working memory in humans. Neurosci Lett 323(2):156–160PubMed Hautzel H, Mottaghy FM, Schmidt D et al (2002) Topographic segregation and convergence of verbal, object, shape and spatial working memory in humans. Neurosci Lett 323(2):156–160PubMed
47.
go back to reference Sperling RA, Bates JF, Chua EF, Cocchiarella AJ, Rentz DM, Rosen BR, Schacter DL, Albert MS (2003) fMRI studies of associative encoding in young and elderly controls and mild Alzheimer’s disease. J Neurol Neurosurg Psychiatry 74(1):44–50CrossRefPubMed Sperling RA, Bates JF, Chua EF, Cocchiarella AJ, Rentz DM, Rosen BR, Schacter DL, Albert MS (2003) fMRI studies of associative encoding in young and elderly controls and mild Alzheimer’s disease. J Neurol Neurosurg Psychiatry 74(1):44–50CrossRefPubMed
48.
go back to reference Maguire EA, Vargha-Khadem F, Mishkin M (2001) The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124(Pt 6):1156–1170CrossRefPubMed Maguire EA, Vargha-Khadem F, Mishkin M (2001) The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124(Pt 6):1156–1170CrossRefPubMed
49.
go back to reference McAllister TW, Sparling MB, Flashman LA, Guerin SJ, Mamourian AC, Saykin AJ (2001) Differential working memory load effects after mild traumatic brain injury. Neuroimage 14(5):1004–1012CrossRefPubMed McAllister TW, Sparling MB, Flashman LA, Guerin SJ, Mamourian AC, Saykin AJ (2001) Differential working memory load effects after mild traumatic brain injury. Neuroimage 14(5):1004–1012CrossRefPubMed
50.
go back to reference Barch DM, Braver TS, Nystrom LE, Forman SD, Noll DC, Cohen JD (1997) Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia 35(10):1373–1380CrossRefPubMed Barch DM, Braver TS, Nystrom LE, Forman SD, Noll DC, Cohen JD (1997) Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia 35(10):1373–1380CrossRefPubMed
51.
go back to reference Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol (Berl) 82:239–259CrossRef Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol (Berl) 82:239–259CrossRef
52.
go back to reference Thal DR, Rub U, Orantes M, Braak H (2002) Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58(12):1791–1800PubMed Thal DR, Rub U, Orantes M, Braak H (2002) Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58(12):1791–1800PubMed
53.
go back to reference Geula C (1998) Abnormalities of neural circuitry in Alzheimer’s disease: hippocampus and cortical cholinergic innervation. Neurology 51(Suppl 1):S18–S29PubMed Geula C (1998) Abnormalities of neural circuitry in Alzheimer’s disease: hippocampus and cortical cholinergic innervation. Neurology 51(Suppl 1):S18–S29PubMed
Metadata
Title
FMRI of working memory in patients with mild cognitive impairment and probable Alzheimer’s disease
Authors
F. Zerrin Yetkin
Roger N. Rosenberg
Myron F. Weiner
Phillip D. Purdy
C. Munro Cullum
Publication date
01-01-2006
Publisher
Springer-Verlag
Published in
European Radiology / Issue 1/2006
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-005-2794-x

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