 |
Previous Article | Next Article 
Volume 17, Number 1,
Issue of January 1, 1997
pp. 391-400
Copyright ©1997 Society for Neuroscience
Age-Related Differences in Neural Activity during Memory Encoding
and Retrieval: A Positron Emission Tomography Study
Received July 31, 1996; revised Oct. 2, 1996; accepted Oct. 3, 1996.
Roberto Cabeza1,
Cheryl
L. Grady1,
Lars Nyberg2,
Anthony R. McIntosh1,
Endel Tulving1,
Shitij Kapur1, 3,
Janine M. Jennings1,
Sylvain Houle3, and
Fergus I. M. Craik1
1 Rotman Research Institute of Baycrest Centre,
University of Toronto, Toronto, Ontario, Canada M6A 2E1,
2 Department of Psychology, University of Umeå, S-90187
Umeå, Sweden, and 3 PET Centre, Clarke Institute of
Psychiatry, University of Toronto, Toronto, Ontario, Canada M6A 2E1
Positron emission tomography (PET) was used to compare regional
cerebral blood flow (rCBF) in young (mean 26 years) and old (mean 70 years) subjects while they were encoding, recognizing, and recalling
word pairs. A multivariate partial-least-squares (PLS) analysis of the
data was used to identify age-related neural changes associated with
(1) encoding versus retrieval and (2) recognition versus recall. Young
subjects showed higher activation than old subjects (1) in left
prefrontal and occipito-temporal regions during encoding and (2) in
right prefrontal and parietal regions during retrieval. Old subjects
showed relatively higher activation than young subjects in several
regions, including insular regions during encoding, cuneus/precuneus
regions during recognition, and left prefrontal regions during recall.
Frontal activity in young subjects was left-lateralized during encoding
and right-lateralized during recall [hemispheric encoding/retrieval
asymmetry (HERA)], whereas old adults showed little frontal activity
during encoding and a more bilateral pattern of frontal activation
during retrieval. In young subjects, activation in recall was higher
than that in recognition in cerebellar and cingulate regions, whereas
recognition showed higher activity in right temporal and parietal
regions. In old subjects, the differences in blood flow between recall and recognition were smaller in these regions, yet more pronounced in
other regions. Taken together, the results indicate that advanced age
is associated with neural changes in the brain systems underlying encoding, recognition, and recall. These changes take two forms: (1)
age-related decreases in local regional activity, which may signal less
efficient processing by the old, and (2) age-related increases in
activity, which may signal functional compensation.
Key words:
positron emission tomography;
cerebral blood flow;
aging;
memory;
encoding;
retrieval;
recognition;
recall;
frontal lobes;
functional reorganization;
functional compensation
This article has been cited by other articles:

|
 |

|
 |
 
J. Ghajar and R. B. Ivry
The Predictive Brain State: Asynchrony in Disorders of Attention?
Neuroscientist,
June 1, 2009;
15(3):
232 - 242.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
G. E. Strangman, R. Goldstein, T. M. O'Neil-Pirozzi, K. Kelkar, C. Supelana, D. Burke, D. I. Katz, S. L. Rauch, C. R. Savage, and M. B. Glenn
Neurophysiological Alterations During Strategy-Based Verbal Learning in Traumatic Brain Injury
Neurorehabil Neural Repair,
March 1, 2009;
23(3):
226 - 236.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Duarte, R. N. Henson, and K. S. Graham
The Effects of Aging on the Neural Correlates of Subjective and Objective Recollection
Cereb Cortex,
September 1, 2008;
18(9):
2169 - 2180.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Ghajar and R. B. Ivry
The Predictive Brain State: Timing Deficiency in Traumatic Brain Injury?
Neurorehabil Neural Repair,
May 1, 2008;
22(3):
217 - 227.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
J. L. Paxton, D. M. Barch, C. A. Racine, and T. S. Braver
Cognitive Control, Goal Maintenance, and Prefrontal Function in Healthy Aging
Cereb Cortex,
May 1, 2008;
18(5):
1010 - 1028.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. W. Davis, N. A. Dennis, S. M. Daselaar, M. S. Fleck, and R. Cabeza
Que PASA? The Posterior-Anterior Shift in Aging
Cereb Cortex,
May 1, 2008;
18(5):
1201 - 1209.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. A. Boyle, R. S. Wilson, J. A. Schneider, J. L. Bienias, and D. A. Bennett
Processing resources reduce the effect of Alzheimer pathology on other cognitive systems
Neurology,
April 22, 2008;
70(17):
1534 - 1542.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Putnam, G. S. Wig, S. T. Grafton, W. M. Kelley, and M. S. Gazzaniga
Structural Organization of the Corpus Callosum Predicts the Extent and Impact of Cortical Activity in the Nondominant Hemisphere
J. Neurosci.,
March 12, 2008;
28(11):
2912 - 2918.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. M. C. Lee, A. W. S. Leung, P. T. Fox, J.-H. Gao, and C. C. H. Chan
Age-related differences in neural activities during risk taking as revealed by functional MRI
Soc Cogn Affect Neurosci,
March 1, 2008;
3(1):
7 - 15.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. R. Wylie, J. J. Foxe, and T. L. Taylor
Forgetting as an Active Process: An fMRI Investigation of Item-Method-Directed Forgetting
Cereb Cortex,
March 1, 2008;
18(3):
670 - 682.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Grady, H. Yu, and C. Alain
Age-Related Differences in Brain Activity Underlying Working Memory for Spatial and Nonspatial Auditory Information
Cereb Cortex,
January 1, 2008;
18(1):
189 - 199.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Morcom, J. Li, and M. D. Rugg
Age Effects on the Neural Correlates of Episodic Retrieval: Increased Cortical Recruitment with Matched Performance
Cereb Cortex,
November 1, 2007;
17(11):
2491 - 2506.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Velanova, C. Lustig, L. L. Jacoby, and R. L. Buckner
Evidence for Frontally Mediated Controlled Processing Differences in Older Adults
Cereb Cortex,
May 1, 2007;
17(5):
1033 - 1046.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Minati, M. Grisoli, and M. G. Bruzzone
MR Spectroscopy, Functional MRI, and Diffusion-Tensor Imaging in the Aging Brain: A Conceptual Review
J Geriatr Psychiatry Neurol,
March 1, 2007;
20(1):
3 - 21.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Maccotta, R. L. Buckner, F. G. Gilliam, and J. G. Ojemann
Changing Frontal Contributions to Memory Before and After Medial Temporal Lobectomy
Cereb Cortex,
February 1, 2007;
17(2):
443 - 456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. J. Sharp, S. K. Scott, M. A. Mehta, and R. J.S. Wise
The Neural Correlates of Declining Performance with Age: Evidence for Age-Related Changes in Cognitive Control
Cereb Cortex,
December 1, 2006;
16(12):
1739 - 1749.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. G. Dobbins and S. Han
Isolating Rule- versus Evidence-Based Prefrontal Activity during Episodic and Lexical Discrimination: a Functional Magnetic Resonance Imaging Investigation of Detection Theory Distinctions
Cereb Cortex,
November 1, 2006;
16(11):
1614 - 1622.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Fridriksson, K. L. Morrow, D. Moser, and G. C. Baylis
Age-Related Variability in Cortical Activity During Language Processing.
J Speech Lang Hear Res,
August 1, 2006;
49(4):
690 - 697.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Persson, L. Nyberg, J. Lind, A. Larsson, L.-G. Nilsson, M. Ingvar, and R. L. Buckner
Structure-Function Correlates of Cognitive Decline in Aging
Cereb Cortex,
July 1, 2006;
16(7):
907 - 915.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Fera, T. W. Weickert, T. E. Goldberg, A. Tessitore, A. Hariri, S. Das, S. Lee, B. Zoltick, M. Meeter, C. E. Myers, et al.
Neural Mechanisms Underlying Probabilistic Category Learning in Normal Aging
J. Neurosci.,
December 7, 2005;
25(49):
11340 - 11348.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. N. Rajah and M. D'Esposito
Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory
Brain,
September 1, 2005;
128(9):
1964 - 1983.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R Vandenberghe and J Tournoy
Cognitive aging and Alzheimer's disease
Postgrad. Med. J.,
June 1, 2005;
81(956):
343 - 352.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. E. Anderson, K. Lynch, E. Zarahn, N. Scarmeas, R. Van Heertum, H. Sackeim, J. R. Moeller, and Y. Stern
H215O PET Study of Impairment of Nonverbal Recognition With Normal Aging
J Neuropsychiatry Clin Neurosci,
May 1, 2005;
17(2):
192 - 200.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Stern, C. Habeck, J. Moeller, N. Scarmeas, K. E. Anderson, H. J. Hilton, J. Flynn, H. Sackeim, and R. van Heertum
Brain Networks Associated with Cognitive Reserve in Healthy Young and Old Adults
Cereb Cortex,
April 1, 2005;
15(4):
394 - 402.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Y. Shan, J. Z. Liu, V. Sahgal, B. Wang, and G. H. Yue
Selective Atrophy of Left Hemisphere and Frontal Lobe of the Brain in Old Men
J. Gerontol. A Biol. Sci. Med. Sci.,
February 1, 2005;
60(2):
165 - 174.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Petrella, B. A. Townsend, A. P. Jha, L. A. Ziajko, M. J. Slavin, C. Lustig, S. J. Hart, and P. M. Doraiswamy
Increasing Memory Load Modulates Regional Brain Activity in Older Adults as Measured by fMRI
J Neuropsychiatry Clin Neurosci,
February 1, 2005;
17(1):
75 - 83.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C Pennanen, C Testa, M P Laakso, M Hallikainen, E-L Helkala, T Hanninen, M Kivipelto, M Kononen, A Nissinen, S Tervo, et al.
A voxel based morphometry study on mild cognitive impairment
J. Neurol. Neurosurg. Psychiatry,
January 1, 2005;
76(1):
11 - 14.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Rossi, C. Miniussi, P. Pasqualetti, C. Babiloni, P. M. Rossini, and S. F. Cappa
Age-Related Functional Changes of Prefrontal Cortex in Long-Term Memory: A Repetitive Transcranial Magnetic Stimulation Study
J. Neurosci.,
September 8, 2004;
24(36):
7939 - 7944.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. W. L. Chee and W. C. Choo
Functional Imaging of Working Memory after 24 Hr of Total Sleep Deprivation
J. Neurosci.,
May 12, 2004;
24(19):
4560 - 4567.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Cabeza, S. M. Daselaar, F. Dolcos, S. E. Prince, M. Budde, and L. Nyberg
Task-independent and Task-specific Age Effects on Brain Activity during Working Memory, Visual Attention and Episodic Retrieval
Cereb Cortex,
April 1, 2004;
14(4):
364 - 375.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Head, R. L. Buckner, J. S. Shimony, L. E. Williams, E. Akbudak, T. E. Conturo, M. McAvoy, J. C. Morris, and A. Z. Snyder
Differential Vulnerability of Anterior White Matter in Nondemented Aging with Minimal Acceleration in Dementia of the Alzheimer Type: Evidence from Diffusion Tensor Imaging
Cereb Cortex,
April 1, 2004;
14(4):
410 - 423.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. J. Madden, W. L. Whiting, J. M. Provenzale, and S. A. Huettel
Age-related Changes in Neural Activity during Visual Target Detection Measured by fMRI
Cereb Cortex,
February 1, 2004;
14(2):
143 - 155.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. Maguire and C. D. Frith
Aging affects the engagement of the hippocampus during autobiographical memory retrieval
Brain,
July 1, 2003;
126(7):
1511 - 1523.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. L. Buckner
Functional-Anatomic Correlates of Control Processes in Memory
J. Neurosci.,
May 15, 2003;
23(10):
3999 - 4004.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Grady, A. R. McIntosh, S. Beig, M. L. Keightley, H. Burian, and S. E. Black
Evidence from Functional Neuroimaging of a Compensatory Prefrontal Network in Alzheimer's Disease
J. Neurosci.,
February 1, 2003;
23(3):
986 - 993.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Gazzaley and M. D'Esposito
The Contribution of Functional Brain Imaging to Our Understanding of Cognitive Aging
Sci. Aging Knowl. Environ.,
January 29, 2003;
2003(4):
pe2 - 2.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
S. M. Daselaar, D. J. Veltman, S. A. R. B. Rombouts, J. G. W. Raaijmakers, and C. Jonker
Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects
Brain,
January 1, 2003;
126(1):
43 - 56.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Morcom, C. D. Good, R. S. J. Frackowiak, and M. D. Rugg
Age effects on the neural correlates of successful memory encoding
Brain,
January 1, 2003;
126(1):
213 - 229.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B Levine, R Cabeza, A R McIntosh, S E Black, C L Grady, and D T Stuss
Functional reorganisation of memory after traumatic brain injury: a study with H2150 positron emission tomography
J. Neurol. Neurosurg. Psychiatry,
August 1, 2002;
73(2):
173 - 181.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V.S. Mattay, F. Fera, A. Tessitore, A.R. Hariri, S. Das, J.H. Callicott, and D.R. Weinberger
Neurophysiological correlates of age-related changes in human motor function
Neurology,
February 26, 2002;
58(4):
630 - 635.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A. Dade, R. J. Zatorre, and M. Jones-Gotman
Olfactory learning: convergent findings from lesion and brain imaging studies in humans
Brain,
January 1, 2002;
125(1):
86 - 101.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Valla, J. D. Berndt, and F. Gonzalez-Lima
Energy Hypometabolism in Posterior Cingulate Cortex of Alzheimer's Patients: Superficial Laminar Cytochrome Oxidase Associated with Disease Duration
J. Neurosci.,
July 1, 2001;
21(13):
4923 - 4930.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Grady, M. L. Furey, P. Pietrini, B. Horwitz, and S. I. Rapoport
Altered brain functional connectivity and impaired short-term memory in Alzheimer's disease
Brain,
April 1, 2001;
124(4):
739 - 756.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. DeCarli, B. L. Miller, G. E. Swan, T. Reed, P. A. Wolf, and D. Carmelli
Cerebrovascular and Brain Morphologic Correlates of Mild Cognitive Impairment in the National Heart, Lung, and Blood Institute Twin Study
Arch Neurol,
April 1, 2001;
58(4):
643 - 647.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Cabeza, S. M. Rao, A. D. Wagner, A. R. Mayer, and D. L. Schacter
Can medial temporal lobe regions distinguish true from false? An event-related functional MRI study of veridical and illusory recognition memory
PNAS,
March 29, 2001;
(2001)
81082698.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
C. Calautti, C. Serrati, and J-C. Baron
Effects of Age on Brain Activation During Auditory-Cued Thumb-to-Index Opposition : A Positron Emission Tomography Study
Stroke,
January 1, 2001;
32(1):
139 - 146.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Della-Maggiore, A. B. Sekuler, C. L. Grady, P. J. Bennett, R. Sekuler, and A. R. McIntosh
Corticolimbic Interactions Associated with Performance on a Short-Term Memory Task Are Modified by Age
J. Neurosci.,
November 15, 2000;
20(22):
8410 - 8416.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Sailer, J. Dichgans, and C. Gerloff
The influence of normal aging on the cortical processing of a simple motor task
Neurology,
October 10, 2000;
55(7):
979 - 985.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Levisohn, A. Cronin-Golomb, and J. D. Schmahmann
Neuropsychological consequences of cerebellar tumour resection in children: Cerebellar cognitive affective syndrome in a paediatric population
Brain,
May 1, 2000;
123(5):
1041 - 1050.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Grady, A. R. McIntosh, M. N. Rajah, S. Beig, and F. I.M. Craik
The Effects of Age on the Neural Correlates of Episodic Encoding
Cereb Cortex,
December 1, 1999;
9(8):
805 - 814.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Backman, J. L. R. Andersson, L. Nyberg, B. Winblad, A. Nordberg, and O. Almkvist
Brain regions associated with episodic retrieval in normal aging and Alzheimer's disease
Neurology,
June 1, 1999;
52(9):
1861 - 1861.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Esposito, B. S. Kirkby, J. D. Van Horn, T. M. Ellmore, and K. F. Berman
Context-dependent, neural system-specific neurophysiological concomitants of ageing: mapping PET correlates during cognitive activation
Brain,
May 1, 1999;
122(5):
963 - 979.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. E. Shaywitz, B. A. Shaywitz, K. R. Pugh, R. K. Fulbright, P. Skudlarski, W. E. Mencl, R. T. Constable, F. Naftolin, S. F. Palter, K. E. Marchione, et al.
Effect of Estrogen on Brain Activation Patterns in Postmenopausal Women During Working Memory Tasks
JAMA,
April 7, 1999;
281(13):
1197 - 1202.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. R. Mcintosh and F. Gonzalez-Lima
Large-Scale Functional Connectivity in Associative Learning: Interrelations of the Rat Auditory, Visual, and Limbic Systems
J Neurophysiol,
December 1, 1998;
80(6):
3148 - 3162.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Cabeza, S. M. Rao, A. D. Wagner, A. R. Mayer, and D. L. Schacter
Can medial temporal lobe regions distinguish true from false? An event-related functional MRI study of veridical and illusory recognition memory
PNAS,
April 10, 2001;
98(8):
4805 - 4810.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|