Skip to main content
PMC home page
Human Brain Mapping logoLink to Human Brain Mapping
. 1999 Feb 1;7(2):115–135. doi: 10.1002/(SICI)1097-0193(1999)7:2<115::AID-HBM5>3.0.CO;2-N

Adult age differences in the functional neuroanatomy of verbal recognition memory

David J Madden 1,✉, Timothy G Turkington 2, James M Provenzale 2, Laura L Denny 1, Thomas C Hawk 2, Lawrence R Gottlob 1, R Edward Coleman 2
PMCID: PMC6873331  PMID: 9950069

Abstract

Adult age differences are frequently observed in the performance of memory tasks, but the changes in neural function mediating these differences are largely unknown. We used H2 15O positron emission tomography (PET) to measure changes in regional cerebral blood flow (rCBF) during Encoding, Baseline, and Retrieval conditions of a recognition memory task. Twelve young adults (20–29 years) and 12 older adults (62–79 years) participated. During each task condition, participants made a two‐choice manual response to each of 64 words. Analyses of the performance data yielded evidence of age‐related slowing of encoding and retrieval processes, and an age‐related decline in the accuracy of yes/no recognition (d'). The rCBF activation associated with both encoding and retrieval was greater for older adults than for young adults, but this pattern was more clearly evident for memory retrieval. For young adults, rCBF activation during retrieval occurred primarily in right prefrontal cortex, whereas older adults exhibited a more bilateral pattern of prefrontal activation. Regression analyses predicting reaction time in the memory task from regional PET counts confirmed that the neural system mediating memory retrieval is more widely distributed for older adults than for young adults. Both age groups exhibited some decrease in rCBF activation in the second half of the test session, relative to the first half. The practice‐related decrease in rCBF activation was more prominent for young adults, suggesting that the older adults' recruitment of additional neural systems reflects a more continual allocation of attention to support task performance. Hum. Brain Mapping 7:115–135, 1999. © 1999 Wiley‐Liss, Inc.

Keywords: neuroimaging, aging, vision, reaction time, information processing, cortical activation

Full Text

The Full Text of this article is available as a PDF (641.0 KB).

REFERENCES

  1. Anderson ND, Craik FIM, Naveh‐Benjamin M. 1998. The attentional demands of encoding and retrieval in younger and older adults: I. Evidence from divided attention costs. Psychol Aging 13:405–423. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=99009512&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  2. Andreasen NC, O'Leary DS, Arndt S, Cizadlo T, Hurtig R, Rezai K, Watkins GL, Boles Ponto LL, Hichwa RD. 1995. Short‐term and long‐term verbal memory: a positron emission tomography study. Proc Natl Acad Sci USA 92:5111–5115. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=95281606&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atkinson RC, Juola JF. 1974. Search and decision processes in recognition memory In: Krantz DH, Atkinson RC, Luce RD, Suppes P, editors. Contemporary developments in mathematical psychology, vol. 1: Learning, memory, and thinking. San Francisco: W.H. Freeman, p 243–293. [Google Scholar]
  4. Bäckman L, Almkvist O, Andersson J, Nordberg A, Winblad B, Reineck R, Langstrom R. 1997. Brain activation in young and older adults during implicit and explicit retrieval. J Cogn Neurosci 9:378–391. [DOI] [PubMed] [Google Scholar]
  5. Badgaiyan RD, Posner MI. 1996. Priming reduces input activity in right posterior cortex during stem completion. NeuroReport 7:2975–2978. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97166371&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  6. Beck AT. 1978. The Beck Depression Inventory. New York: Psychological Corporation. [Google Scholar]
  7. Buckner RL. 1996. Beyond HERA: contributions of specific prefrontal brain areas to long‐term memory retrieval. Psychon Bull Rev 3:149–158. [DOI] [PubMed] [Google Scholar]
  8. Buckner RL, Tulving E. 1995. Neuroimaging studies of memory: theory and recent PET results In: Boller F, Grafman J, editors. Handbook of neuropsychology, vol 10 Amsterdam: Elsevier; p 439–466. [Google Scholar]
  9. Buckner RL, Petersen SE, Ojemann JG, Miezin FM, Squire LR, Raichle ME. 1995. Functional anatomical studies of explicit and implicit memory retrieval tasks. J Neurosci 15:12–29. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=95123435&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Burke DM, Light LL. 1981. Memory and aging: the role of retrieval processes. Psychol Bull 90:513–546. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=82060903&form=6&db=m&Dopt=r [PubMed] [Google Scholar]
  11. Cabeza R, Nyberg L. 1997. Imaging cognition: an empirical review of PET studies with normal subjects. J Cogn Neurosci 9:1–26. [DOI] [PubMed] [Google Scholar]
  12. Cabeza R, Grady CL, Nyberg L, McIntosh AR, Tulving E, Kapur S, Jennings JM, Houle S, Craik FIM. 1997. Age‐related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J Neurosci 17:391–400. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97141578&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Carroll JB, Davies P, Richman B. 1971. The American Heritage word frequency book. New York: American Heritage. [Google Scholar]
  14. Cerella J. 1990. Aging and information‐processing rate In: Birren JE, Schaie KW, editors. Handbook of the psychology of aging, 3rd ed San Diego: Academic; p 201–221. [Google Scholar]
  15. Christensen KJ, Moye J, Armson RR, Kern TM. 1992. Health screening and random recruitment for cognitive aging research. Psychol Aging 7:204–208. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=92304486&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Craik FIM. 1977. Age differences in human memory In: Birren JE, Schaie KW, editors. Handbook of the psychology of aging. New York: Van Nostrand Reinhold; p 384–420. [Google Scholar]
  17. Craik FIM, Jennings JM. 1992. Human memory In: Craik FIM, Salthouse TA, editors. The handbook of aging and cognition. Hillsdale: N.J.: Erlbaum; p 51–110. [Google Scholar]
  18. Craik FIM, Lockhart RS. 1972. Levels of processing: a framework for memory research. J Verb Learn Verb Behav 11:671–684. [Google Scholar]
  19. Craik FIM, McDowd JM. 1987. Age differences in recall and recognition. J Exp Psychol [Learn Mem Cogn] 13:474–479. [Google Scholar]
  20. Craik FIM, Tulving E. 1975. Depth of processing and the retention of words in episodic memory. J Exp Psychol [General] 104:268–294. [Google Scholar]
  21. DeGrado TR, Turkington TG, Williams JJ, Stearns CW, Hoffman JM, Coleman RE. 1994. Performance characteristics of a whole‐body PET scanner. J Nucl Med 35:1398–1406. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94322107&form=6&db=m&Dopt=r [PubMed] [Google Scholar]
  22. Erber J. 1974. Age differences in recognition memory. J Gerontol 29:177–181. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=74092316&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  23. 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 12:189–198. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=76071605&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  24. Friston KJ, Frith CD, Liddle PF, Dolan RJ, Lammertsma AA, Frackowiak RSJ. 1990. The relationship between global and local changes in PET scans. J Cereb Blood Flow Metab 10:458–466. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=90270299&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  25. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ. 1995. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapping 2:189–210. [Google Scholar]
  26. Friston KJ, Ashburner J, Poline JB, Frith CD, Heather JD, Frackowiak RSJ. 1996. Spatial realignment and normalization of images. Hum Brain Mapping 3:165–189. [Google Scholar]
  27. Goldman‐Rakic PS. 1987. Circuitry of primate prefrontal cortex and regulation of behavior by representational memory In: Mountcastle VB, Plum F, editors. Handbook of physiology, section 1: The nervous system, vol. 5. Bethesda Md.: American Physiological Society; p 373–417. [Google Scholar]
  28. Gordon SK, Clark WC. 1974. Application of signal detection theory to prose recall and recognition in elderly and young adults. J Gerontol 29:64–72. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=74071731&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  29. Grady CL, Maisog JM, Horwitz B, Ungerleider LG, Mentis MJ, Salerno JA, Pietrini P, Wagner E, Haxby JV. 1994. Age‐related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci 14:1450–1462. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94172435&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Grady CL, McIntosh AR, Horwitz B, Maisog JM, Ungerleider LG, Mentis MJ, Pietrini P, Schapiro MB, Haxby JV. 1995. Age‐related reductions in human recognition memory due to impaired encoding. Science 269:218–221. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=95343342&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  31. Grady CL, Horwitz B, Pietrini P, Mentis MJ, Ungerleider LG, Rapoport SI, Haxby JV. 1996. Effect of task difficulty on cerebral blood flow during perceptual matching of faces. Hum Brain Mapping 4:227–239. [DOI] [PubMed] [Google Scholar]
  32. Haxby JV, Grady CL, Horwitz B, Salerno J, Ungerleider LG, Mishkin M, Shapiro MB, Rapaport SI. 1993. Dissociation of object and spatial visual processing pathways in human extrastriate cortex In: Gulyas B, Ottoson D, Roland PE, editors. Functional organisation of the human visual cortex. Oxford: Pergamon Press; p 329–340. [Google Scholar]
  33. Kausler DH. 1994. Learning and memory in normal aging. New York: Academic. [Google Scholar]
  34. Kinahan PE, Rogers JG. 1990. Analytic 3D image reconstruction using all detected events. IEEE Trans Nucl Sci 37:773–777. [Google Scholar]
  35. LaBerge D. 1995. Computational and anatomical models of selective attention in object identification In: Gazzaniga MS, editor. The cognitive neurosciences. Cambridge Mass.: MIT Press; p 649–663. [Google Scholar]
  36. Leiner HC, Leiner HC, Dow RS. 1995. The underestimated cerebellum. Hum Brain Mapping 2:244–254. [Google Scholar]
  37. Light LL. 1991. Memory and aging: Four hypotheses in search of data. Ann Rev Psychol 42:333–376. [DOI] [PubMed] [Google Scholar]
  38. Littell RC, Milliken GA, Stroup GA, Wolfinger RD. 1996. SAS system for mixed models. Cary, N.C.: SAS Institute. [Google Scholar]
  39. Madden DJ. 1986. Adult age differences in visual word recognition: semantic encoding and episodic retention. Exp Aging Res 12:71–78. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=87190628&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  40. Madden DJ, Turkington TG, Coleman RE, Provenzale JM, DeGrado TR, Hoffman JM. 1996. Adult age differences in regional cerebral blood flow during visual word identification: evidence from H2 15O PET. NeuroImage 3:127–142. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=98005344&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  41. Mandler GM. 1980. Recognizing: the judgment of previous occurrence. Psychol Rev 87:252–271. [Google Scholar]
  42. McNicol D. 1972. A primer of signal detection theory. London: Allen and Unwin. [Google Scholar]
  43. Myerson J, Hale S, Wagstaff D, Poon LW, Smith GA. 1990. The information loss model: a mathematical theory of age‐related cognitive slowing. Psychol Rev 97:475–487. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=91062493&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  44. Neter J, Wasserman W, Kutner MH. 1990. Applied linear statistical models: regression, analysis of variance, and experimental designs, 3rd ed. Homewood, Ill.: Irwin. [Google Scholar]
  45. Nyberg L, Tulving E, Habib R, Nilsson L‐G, Kapur S, Houle S, Cabeza R, McIntosh AR. 1995. Functional brain maps of retrieval mode and recovery of episodic information. NeuroReport 7:249–252. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96352205&form=6&db=m&Dopt=r [PubMed] [Google Scholar]
  46. Nyberg L, Cabeza R, Tulving E. 1996a. PET studies of encoding and retrieval: the HERA model. Psychon Bull Rev 3:135–148. [DOI] [PubMed] [Google Scholar]
  47. Nyberg L, McIntosh AR, Cabeza R, Nilsson L‐G, Houle S, Habib R, Tulving E. 1996b. Network analysis of positron emission tomography regional cerebral blood flow data: Ensemble inhibition during episodic memory retrieval. J Neurosci 16:3753–3759. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96221435&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Parks TE. 1966. Signal‐detectability theory of recognition‐memory performance. Psychol Rev 73:44–58. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=66097844&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  49. Perlmutter M. 1979. Age differences in adults' free recall, cued recall, and recognition. J Gerontol 34:533–539. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=79194902&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  50. Petersen SE, Fox PT, Snyder AZ, Raichle ME. 1990. Activation of extrastriate and frontal cortical areas by visual words and word‐like stimuli. Science 249:1041–1044. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=90371300&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  51. Rabinowitz JC. 1989. Age deficits in recall under optimal study conditions. Psychol Aging 4:378–380. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=90027487&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  52. Raichle ME, Fiez JA, Videen TO, MacLeod AK, Pardo JV, Fox PT, Petersen SE. 1994. Practice‐related changes in human brain functional anatomy during nonmotor learning. Cereb Cortex 4:8–26. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94235980&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  53. Ratcliff R. 1978. A theory of memory retrieval. Psychol Rev 85:59–108. [Google Scholar]
  54. Raz N, Gunning FM, Head D, Dupuis JH, McQuain J, Briggs SD, Loken WJ, Thornton AE, Acker JD. 1997. Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex 7:268–282. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97288468&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  55. Raz N, Gunning‐Dixon FM, Head D, Dupuis JH, Acker JD. 1998. Neuroanatomical correlates of cognitive aging: evidence from structural MRI. Neuropsychology 12:95–114. [DOI] [PubMed] [Google Scholar]
  56. Rugg MD, Fletcher PC, Frith CD, Frackowiak RSJ, Dolan RJ. 1996. Differential activation of the prefrontal cortex in successful and unsuccessful memory retrieval. Brain 119:2073–2083. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97163176&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  57. Rugg MD, Fletcher PC, Frith CD, Frackowiak RSJ, Dolan RJ. 1997. Brain regions supporting intentional and incidental memory: a PET study. NeuroReport 8:1283–1287. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97318147&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  58. Salthouse TA. 1982. Adult cognition: an experimental psychology of human aging. New York: Springer‐Verlag. [Google Scholar]
  59. Salthouse TA. 1991. Theoretical perspectives on cognitive aging. Hillsdale, N.J.: Erlbaum. [Google Scholar]
  60. Salthouse TA. 1996. The processing‐speed theory of adult age differences in cognition. Psychol Rev 103:403–428. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96321875&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  61. Schacter DL, Savage CR, Alpert NM, Rauch SL, Albert MS. 1996. The role of hippocampus and frontal cortex in age‐related memory changes: a PET study. NeuroReport 7:1165–1169. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=96414504&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  62. Schacter DL, Buckner RL, Koutstaal W, Dale AM, Rosen BR. 1997. Late onset of anterior prefrontal activity during true and false recognition: an event‐related fMRI study. NeuroImage 6:259–269. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=98080650&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  63. Schmahmann JD. 1996. From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Hum Brain Mapping 4:174–198. [DOI] [PubMed] [Google Scholar]
  64. Shulman GL, Corbetta M, Buckner RL, Raichle ME, Fiez JA, Miezin FM, Petersen SE. 1997. Top‐down modulation of early sensory cortex. Cereb Cortex 7:193–206. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97288463&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  65. Smith AD. 1996. Memory In: Birren JE, Schaie KW, editors. Handbook of the psychology of aging, 4th ed San Diego: Academic; p 236–250. [Google Scholar]
  66. Smith ME, Halgren E. 1989. Dissociation of recognition memory components following temporal lobe lesions. J Exp Psychol [Learn Mem Cogn] 15:50–60. [DOI] [PubMed] [Google Scholar]
  67. Snodgrass JG, Corwin J. 1988. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J Exp Psychol [General] 117:34–50. [DOI] [PubMed] [Google Scholar]
  68. Squire LR, Ojemann JG, Miezin FM, Petersen SE, Videen TO, Raichle ME. 1992. Activation of the hippocampus in normal humans: a functional anatomical study of memory. Proc Natl Acad Sci USA 89:1837–1841. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=92179277&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Talairach J, Tournoux P. 1988. Co‐planar stereotaxic atlas of the human brain. Stuttgart: Thieme. [Google Scholar]
  70. Tulving E, Kapur S, Craik FIM, Moscovitch M, Houle S. 1994a. Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc Natl Acad Sci USA 91:2016–2020. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94181522&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Tulving E, Kapur S, Markowitsch HJ, Craik FIM, Habib R, Houle S. 1994b. Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. Proc Natl Acad Sci USA 91:2012–2015. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=94181521&form=6&db=m&Dopt=r [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Ungerleider LG, Mishkin M. 1982. Two cortical visual systems In: Ingle DJ, Goodale MA, Mansfield RJW, editors. Analysis of visual behavior. Cambridge Mass.: MIT Press; p 549–586. [Google Scholar]
  73. Wechsler D. 1981. Wechsler Adult Intelligence Scale‐Revised. New York: Psychological Corporation. [Google Scholar]
  74. Whiting WL, Smith AD. 1997. Differential age‐related processing limitations in recall and recognition tasks. Psychol Aging 12:216–224. http://www.ncbi.nlm.nih.gov:80/htbin-post/Entrez/query?uid=97333856&form=6&db=m&Dopt=r [DOI] [PubMed] [Google Scholar]
  75. Yonelinas AP. 1994. Receiver‐operating characteristics in recognition memory: evidence for a dual‐process model. J Exp Psychol [Learn Mem Cogn] 20:1341–1354. [DOI] [PubMed] [Google Scholar]
  76. Yonelinas AP. 1997. Recognition memory ROCs for item and associative information: the contribution of recollection and familiarity. Mem Cogn 25:747–763. [DOI] [PubMed] [Google Scholar]

Articles from Human Brain Mapping are provided here courtesy of Wiley

RESOURCES