The impact of age on prefrontal cortex integrity during spatial working memory retrieval

Neuropsychologia

Volumn 59, Issue 1, 2014, Pages 157-168

  Toepper, Max ^a,b   Markowitsch, Hans J ^c   Gebhardt, Helge ^b   Beblo, Thomas ^a   Bauer, Eva ^b   Woermann, Friedrich G ^d   Driessen, Martin ^a   Sammer, Gebhard ^b  

^a EVANGELISCHES KRANKENHAUS   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

^d EPILEPSY CENTER BETHEL   (Germany)

Author keywords

Aging; Cognitive control; Dorsolateral prefrontal cortex; Functional connectivity; Retrieval; Working memory

Indexed keywords

ACCURACY; ADULT; AGE DISTRIBUTION; AGING; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; BRAIN REGION; CONNECTOME; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFORMATION STORAGE; MALE; MEMORY CONSOLIDATION; ORBITAL CORTEX; PREFRONTAL CORTEX; RIGHT HEMISPHERE; SPATIAL MEMORY; TASK PERFORMANCE; WORKING MEMORY; AGED; MIDDLE AGED; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; REACTION TIME; SHORT TERM MEMORY; SIGNAL PROCESSING; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; AGING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; REACTION TIME; SIGNAL PROCESSING, COMPUTER-ASSISTED; SPATIAL MEMORY; YOUNG ADULT;

EID: 84901478450     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2014.04.020     Document Type: Article

References (99)

1. Amaro E., Barker G.J. Study design in fMRI: basic principles. Brain and Cognition 2006, 60:220-232.
2. Baddeley A.D. Working memory 1986, Oxford University Press, Oxford.
3. Badre D., D'Esposito M. Is the rostro-caudal axis of the frontal lobe hierarchical?. Nature Reviews Neuroscience 2009, 10:659-669.
4. Bennett I.J., Rivera H.G., Rypma B. Isolating age-group differences in working memory load-related neural activity: Assessing the contribution of working memory capacity using a partial-trial fMRI method. Neuroimage 2013, 72:20-32.
5. Blumenfeld R.S., Nomura E.M., Gratton C., D'Esposito M. Lateral prefrontal cortex is organized into parallel dorsal and ventral streams along the rostro-caudal axis. Cerebral Cortex 2013, 23:2457-2466.
6. Bor D., Duncan J., Lee A.C., Parr A., Owen A.M. Frontal lobe involvement in spatial span: Converging studies of normal and impaired function. Neuropsychologia 2006, 44:229-237.
7. Buckley M.J., Mansouri F.A., Hoda H., Mahboubi M., Browning P.G., Kwok S.C., et al. Dissociable components of rule-guided behavior depend on distinct medial and prefrontal regions. Science 2009, 325:52-58.
8. Cabeza R. Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychology and Aging 2002, 17:85-100.
9. Cabeza R., Daselaar S.M., Dolcos F., Prince S.E., Budde M., Nyberg L. Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cerebral Cortex 2004, 14:364-375.
10. Cabeza R., Nyberg L. Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience 2000, 12:1-47.
11. Campbell K.L., Grady C.L., Ng C., Hasher L. Age differences in the frontoparietal cognitive control network: Implications for distractibility. Neuropsychologia 2012, 50:2212-2222.
12. Cappell K.A., Gmeindl L., Reuter-Lorenz P.A. Age differences in prefrontal recruitment during verbal working memory maintenance depend on memory load. Cortex 2010, 46:462-473.
13. Carp J., Gmeindl L., Reuter-Lorenz P.A. Age differences in the neural representation of working memory revealed by multi-voxel pattern analysis. Frontiers in Human Neuroscience 2010, 4:217.
14. Christoff K., Gabrieli J.D. The frontopolar Cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex. Psychobiology 2000, 28:168-186.
15. Courtney S.M., Petit L., Maisog J.M., Ungerleider L.G., Haxby J.V. An area specialized for spatial working memory in human frontal cortex. Science 1998, 279:1347-1351.
16. Corsi P.M. Human memory and the medial temporal region of the brain. Dissertation Abstracts International 1972, 34:819B.
17. Davis S.W., Dennis N.A., Daselaar S.M., Fleck M.S., Cabeza R. Que PASA? The posterior-anterior shift in aging. Cerebral Cortex 2008, 18:1201-1209.
18. De Beni R., Palladino P. Decline in working memory updating through ageing: Intrusion error analyses. Memory 2004, 12:75-89.
19. Deco G., Rolls E.T., Horwitz B. "What" and "where" in visual working memory: A computational neurodynamical perspective for integrating fMRI and single-neuron data. Journal of Cognitive Neuroscience 2004, 16:683-701.
20. D'Esposito M., Postle B.R., Ballard D., Lease J. Maintenance versus manipulation of information held in working memory: An event-related fMRI study. Brain and Cognition 1999, 41:66-86.
21. Esslinger C., Walter H., Kirsch P., Erk S., Schnell K., Arnold C., et al. Neural mechanisms of a genome-wide supported psychosis variant. Science 2009, 324:605.
22. Fjell A.M., Walhovd K.B. Structural brain changes in aging: courses, causes and cognitive consequences. Reviews in the Neurosciences 2010, 21:187-221.
23. Folstein M.F., Folstein S.E., McHugh P.R. 'Mini-mental state'. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 1975, 12:189-198.
24. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
25. Grady C.L., Protzner A.B., Kovacevic N., Strother S.C., Afshin-Pour B., Wojtowicz M., et al. A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. Cerebral Cortex 2010, 20:1432-1447.
26. Gutchess A.H., Welsh R.C., Hedden T., Bangert A., Minear M., Liu L.L., et al. Aging and the neural correlates of successful picture encoding: Frontal activations for decreased medial temporal activity. Journal of Cognitive Neuroscience 2005, 17:84-96.
27. Holtzer R., Rakitin B.C., Steffener J., Flynn J., Kumar A., Stern Y. Age effects on load-dependent brain activations in working memory for novel material. Brain Research 2009, 1249:148-161.
28. Johnson M.K., Mitchell K.J., Raye C.L., Greene E.J. An age-related deficit in prefrontal cortical function associated with refreshing information. Psychological Science 2004, 15:127-132.
29. Jolles D.D., van Buchem M.A., Crone E.A., Rombouts S.A. Functional brain connectivity at rest changes after working memory training. Human Brain Mapping 2013, 34:396-406.
30. Jonides J., Marshuetz C., Smith E.E., Reuter-Lorenz P.A., Koeppe R.A., Hartley A. Age differences in behavior and PET activation reveal differences in interference resolution in verbal working memory. Journal of Cognitive Neuroscience 2000, 12:188-196.
31. Jonides J., Nee D.E. Brain mechanisms of proactive interference in working memory. Neuroscience 2006, 139:181-193.
32. Kaplan E., Goodglass H., Weintraub S. Boston naming test 1983, Lea & Febiger, Philadelphia.
33. Kennedy K.M., Raz N. Aging white matter and cognition: Differential effects of regional variations in diffusion properties on memory, executive functions, and speed. Neuropsychologia 2009, 47:916-927.
34. Kessler J., Calabrese P., Kalbe E., Berger F. DemTect: A new screening method to support diagnosis of dementia. Psychologie 2000, 26:343-347.
35. Klostermann E.C., Braskie M.N., Landau S.M., O'Neil J.P., Jagust W.J. Dopamine and frontostriatal networks in cognitive aging. Neurobiology of Aging 2012, 33:15-24.
36. Kumar A., Foster T.C. Neurophysiology of old neurons and synapses. Brain aging: Models, methods, and mechanisms 2007, CRC Press, Boca Raton. D.R. Riddle (Ed.).
37. Kwok S.C., Shallice T., Macaluso E. Functional anatomy of temporal organisation and domain-specificity of episodic memory retrieval. Neuropsychologia 2012, 50:2943-2955.
38. Lancaster J.L., Rainey L.H., Summerlin J.L., Freitas C.S., Fox P.T., Evans A.C., et al. Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward-transform method. Human Brain Mapping 1997, 5:238-242.
39. Lancaster J.L., Woldorff M.G., Parsons L.M., Liotti M., Freitas C.S., Rainey L., et al. Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping 2000, 10:120-131.
40. Lezak M.D., Howieson D.B., Loring D.W. Neuropsychological assessment 2004, Oxford University Press, New York. 4th ed.
41. Li K., Guo L., Nie J., Li G., Liu T. Review of methods for functional brain connectivity detection using fMRI. Computerized Medical Imaging and Graphics 2009, 33:131-139.
42. Madden D.J., Costello M.C., Dennis N.A., Davis S.W., Shepler A.M., Spaniol J., et al. Adult age differences in functional connectivity during executive control. Neuroimage 2010, 52:643-657.
43. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
44. Mattay V.S., Fera F., Tessitore A., Hariri A.R., Berman K.F., Das S., et al. Neurophysiological correlates of age-related changes in working memory capacity. Neuroscience Letters 2006, 392:32-37.
45. Matthäus F., Schmidt J.P., Banerjee A., Schulze T.G., Demirakca T., Diener C. Effects of age on the structure of functional connectivity networks during episodic and working memory demand. Brain Connectivity 2012, 2:113-124.
46. Meyer-Lindenberg A. Neural connectivity as an intermediate phenotype: Brain networks under genetic control. Human Brain Mapping 2009, 30:1938-1946.
47. Montembeault M., Joubert S., Doyon J., Carrier J., Gagnon J.F., Monchi O., et al. The impact of aging on gray matter structural covariance networks. Neuroimage 2012, 63:754-759.
48. Motes M.A., Rypma B. Working memory component processes: Isolating BOLD signal changes. Neuroimage 2010, 49:1933-1941.
49. Müller H., Hasse-Sander I., Horn R., Helmstaedter C., Elger C.E. Rey auditory-verbal learning test: Structure of a modified German version. Journal of Clinical Psychology 1997, 53:663-671.
50. Nagel I.E., Preuschhof C., Li S.C., Nyberg L., Bäckman L., Lindenberger U., et al. Performance level modulates adult age differences in brain activation during spatial working memory. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:22552-22557.
51. Nagel I.E., Preuschhof C., Li S.C., Nyberg L., Bäckman L., Lindenberger U., et al. Load modulation of BOLD response and connectivity predicts working memory performance in younger and older adults. Journal of Cognitive Neuroscience 2011, 23:2030-2045.
52. Nee D.E., Brown J.W. Rostral-caudal gradients of abstraction revealed by multi-variate pattern analysis of working memory. Neuroimage 2012, 63:1285-1294.
53. Nee D.E., Brown J.W., Askren M.K., Berman M.G., Demiralp E., Krawitz A., et al. A meta-analysis of executive components of working memory. Cerebral Cortex 2013, 23:264-282.
54. Owen A.M. The functional organization of working memory processes within human lateral frontal cortex: The contribution of functional neuroimaging. European Journal of Neuroscience 1997, 9:1329-1339.
55. Owen A.M., Evans A.C., Petrides M. Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: A positron emission tomography study. Cerebral Cortex 1996, 6:31-38.
56. Owen A.M., Herrod N.J., Menon D.K., Clark J.C., Downey S.P., Carpenter T.A., et al. Redefining the functional organization of working memory processes within human lateral prefrontal cortex. European Journal of Neuroscience 1999, 11:567-574.
57. Park D.C., Lautenschlager G., Hedden T., Davidson N.S., Smith A.D., Smith P.K. Models of visuospatial and verbal memory across the adult life span. Psychology and Aging 2002, 17:299-320.
58. Park D.C., Polk T.A., Park R., Minear M., Savage A., Smith M.R. Aging reduces neural specialization in ventral visual cortex. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:13091-13095.
59. Park D.C., Reuter-Lorenz P.A. The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology 2009, 60:173-196.
60. Persson J., Sylvester C.Y., Nelson J.K., Welsh K.M., Jonides J., Reuter-Lorenz P.A. Selection requirements during verb generation: Differential recruitment in older and younger adults. Neuroimage 2004, 23:1382-1390.
61. Petrides M. Functional organization of the human frontal cortex for mnemonic processing. Evidence from neuroimaging studies. Annals of the New York Academy of Sciences 1995, 769:85-96.
62. Rabbitt P., Ibrahim S., Lunn M., Scott M., Thacker N., Hutchinson C., et al. Age-associated losses of brain volume predict longitudinal cognitive declines over 8 to 20 years. Neuropsychology 2008, 22:3-9.
63. Rajah M.N., D'Esposito M. Region-specific changes in prefrontal function with age: A review of PET and fMRI studies on working and episodic memory. Brain 2005, 128:1964-1983.
64. Raz N. Aging of the brain and its impact on cognitive performance: Integration of structural and functional findings. Handbook of aging and cognition - II 2008, 1-90. Erlbaum, Mahwah. F.I. M. Craik, T.A. Salthouse (Eds.).
65. Raz N., Gunning F.M., Head D., Dupuis J.H., McQuain J., Briggs S.D., et al. Selective aging of the human cerebral cortex observed in vivo: Differential vulnerability of the prefrontal grey matter. Cerebral Cortex 1997, 7:268-282.
66. Reitan R.M. The relation of the trail making test to organic brain damage. Journal of Consulting Psychology 1955, 19:393-394.
67. Resnick S.M., Pham D.L., Kraut M.A., Zonderman A.B., Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: A shrinking brain. Journal of Neuroscience 2003, 23:3295-3301.
68. Reuter-Lorenz P.A., Cappell K.A. Neurocognitive aging and the compensation hypothesis. Current Directions in Psychological Science 2008, 17:177-182.
69. Reuter-Lorenz P.A., Jonides J., Smith E.E., Hartley A., Miller A., Marshuetz C., et al. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. Journal of Cognitive Neuroscience 2000, 12:174-187.
70. Reuter-Lorenz P.A., Lustig C. Brain aging: Reorganizing discoveries about the aging mind. Current Opinion in Neurobiology 2005, 15:245-251.
71. Reuter-Lorenz P.A., Park D.C. Human neuroscience and the aging mind: A new look at old problems. The Journals of Gerontology Series B: Psychological Sciences and Social Sciences 2010, 65:405-415.
72. Reuter-Lorenz P.A., Sylvester C.Y. The cognitive neuroscience of working memory and aging. Cognitive neuroscience of aging: Linking cognitive and cerebral aging 2005, 186-217. Oxford University Press, New York. R. Cabeza, L. Nyberg, D. Park (Eds.).
73. Rieckmann A., Karlsson S., Fischer H., Bäckman L. Caudate dopamine D1 receptor density is associated with individual differences in frontoparietal connectivity during working memory. Journal of Neuroscience 2011, 31:14284-14290.
74. Roth J.K., Serences J.T., Courtney S.M. Neural system for controlling the contents of object working memory in humans. Cerebral Cortex 2006, 16:1595-1603.
75. Rottschy C., Langner R., Dogan I., Reetz K., Laird A.R., Schulz J.B., et al. Modelling neural correlates of working memory: A coordinate-based meta-analysis. Neuroimage 2012, 60:830-846.
76. Rypma B., Berger J.S., D'Esposito M. The influence of working-memory demand and subject performance on prefrontal cortical activity. Journal of Cognitive Neuroscience 2002, 14:721-731.
77. Rypma B., Berger J.S., Genova H.M., Rebbechi D., D'Esposito M. Dissociating age-related changes in cognitive strategy and neural efficiency using event-related fMRI. Cortex 2005, 41:582-594.
78. Rypma B., D'Esposito M. Isolating the neural mechanisms of age-related changes in human working memory. Nature Neuroscience 2000, 3:509-515.
79. Rypma B., Prabhakaran V., Desmond J.E., Gabrieli J.D. Age differences in prefrontal cortical activity in working memory. Psychology and Aging 2001, 16:371-384.
80. Sambataro F., Murty V.P., Callicott J.H., Tan H.Y., Das S., Weinberger D.R., et al. Age-related alterations in default mode network: Impact on working memory performance. Neurobiology of Aging 2010, 31:839-852.
81. Sander M.C., Lindenberger U., Werkle-Bergner M. Lifespan age differences in working memory: A two-component framework. Neuroscience & Biobehavioral Reviews 2012, 36:2007-2033.
82. Sandrini M., Rossini P.M., Miniussi C. Lateralized contribution of prefrontal cortex in controlling task-irrelevant information during verbal and spatial working memory tasks: rTMS evidence. Neuropsychologia 2008, 46:2056-2063.
83. Schneider-Garces N.J., Gordon B.A., Brumback-Peltz C.R., Shin E., Lee Y., Sutton B.P., et al. Span, CRUNCH, and beyond: Working memory capacity and the aging brain. Journal of Cognitive Neuroscience 2010, 22:655-669.
84. Schröder M.R., Hasse-Sander I., Müller H., Horn R., Möller H.J. Merkmalsanalyse von Uhrzeichnungen als Beitrag zur Diagnostik der Demenz vom Alzheimer Typ (DAT). Zeitschrift für Gerontopsychologie & -psychiatrie 1999, 12:55-66.
85. Seidler R.D., Bernard J.A., Burutolu T.B., Fling B.W., Gordon M.T., Gwin J.T., et al. Motor control and aging: Links to age-related brain structural, functional, and biochemical effects. Neuroscience & Biobehavioral Reviews 2010, 34:721-731.
86. Shulman K.I., Gold D.P., Cohen C.A., Zucchero C.A. Clock-drawing and dementia in the community: A longitudinal study. International Journal of Geriatric Psychiatry 1993, 8:487-496.
87. Smith E.E., Jonides J. Working memory: A view from neuroimaging. Cognitive Psychology 1997, 33:5-42.
88. Smith E.E., Jonides J. Storage and executive processes in the frontal lobes. Science 1999, 283:1657-1661.
89. Steffener J., Habeck C.G., Stern Y. Age-related changes in task related functional network connectivity. PLoS One 2012, 7:e44421.
90. Talairach J., Tournoux P. Co-planar stereotactic atlas of the human brain: 3-Dimensional proportional system: an approach to cerebral imaging 1998, Thieme, Stuttgart.
91. Thomsen T., Specht K., Hammar A., Nyttingnes J., Ersland L., Hugdahl K. Brain localization of attentional control in different age groups by combining functional and structural MRI. Neuroimage 2004, 22:912-919.
92. Toepper M., Gebhardt H., Beblo T., Thomas C., Driessen M., Bischoff M., et al. Functional correlates of distractor suppression during spatial working memory encoding. Neuroscience 2010, 165:1244-1253.
93. Toepper M., Markowitsch H.J., Gebhardt H., Beblo T., Thomas C., Gallhofer B., et al. Hippocampal involvement in working memory encoding of changing locations: An fMRI study. Brain Research 2010, 1354:91-99.
94. Toepper M., Markowitsch H.J., Kater L., Gebhardt H., Beblo T., Bauer E., et al. Neural correlates of impaired inhibitory processes in mild cognitive impairment. Behavioural Neurology 2013, 3:27.
95. Tombaugh T.N. Trail Making Test A and B: Normative data stratified by age and education. Archives of Clinical Neuropsychology 2004, 19:203-214.
96. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
97. Wagner A.D., Maril A., Bjork R.A., Schacter D.L. Prefrontal contributions to executive control: fMRI evidence for functional distinctions within lateral prefrontal cortex. Neuroimage 2001, 14:1337-1347.
98. Wilson R.C., Takahashi Y.K., Schoenbaum G., Niv Y. Orbitofrontal cortex as a cognitive map of task space. Neuron 2014, 81:267-279.
99. Zarahn E., Rakitin B., Abela D., Flynn J., Stern Y. Age-related changes in brain activation during a delayed item recognition task. Neurobiology of Aging 2007, 28:784-798.