Differential Effects of Normal Aging on Memory for Odor-Place and Object-Place Associations

REFERENCES

• Astur , R. S. , Taylor , L. B. , Mamelak , A. N. , Philpott , L. , & Sutherland , R. J. ( 2002 ). Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task . Behavioral Brain Research , 132 , 77 – 84 .
   PubMed Web of Science ®Google Scholar
• Bastin , C. & Van der Linden , M. ( 2006 ). The effects of aging on the recognition of different types of associations . Experimental Aging Research , 32 , 61 – 77 .
   PubMed Web of Science ®Google Scholar
• Bhatnagar , K. P. , Kennedy , R. C. , Baron , G. , & Greenberg , R. A. ( 1987 ). Number of mitral cells and the bulb volume in the aging human olfactory bulb: A quantitative morphological study . Anatomical Record , 218 , 73 – 87 .
   PubMedGoogle Scholar
• Bohbot , V. D. , Jech , R. , Ruzicka , E. , Nadel , L. , Kalina , M. , Stepankova , K. , & Bures , J. ( 2002 ). Rat spatial memory tasks adapted for humans: Characterization in subjects with intact brain and subjects with selective medial temporal lobe thermal lesions . Physiological Research , 51 (Suppl 1) , 49 – S65 .
   PubMedGoogle Scholar
• Castel , A. D. & Craik , F. I. ( 2003 ). The effects of aging and divided attention on memory for item and associative information . Psychology and Aging , 18 , 873 – 885 .
   PubMed Web of Science ®Google Scholar
• Cerf-Ducastel , B. & Murphy , C. ( 2001 ). fMRI activation in response to odorants orally delivered in aqueous solutions . Chemical Senses , 26 , 625 – 637 .
   PubMedGoogle Scholar
• Cerf-Ducastel , B. & Murphy , C. ( 2003 ). fMRI brain activation in response to odors is reduced in primary olfactory areas of elderly subjects . Brain Research , 986 , 39 – 53 .
   PubMed Web of Science ®Google Scholar
• Cerf-Ducastel , B. & Murphy , C. ( 2006 ). Neural substrates of cross-modal olfactory recognition memory: An fMRI study . Neuroimage , 31 , 386 – 396 .
   PubMed Web of Science ®Google Scholar
• Coffey , C. E. , Wilkinson , W. E. , Parashos , I. A. , Soady , S. A. R. , Sullivan , R. J. , Patterson , L. J. , Figiel , G. S. , Webb , M. C. , Spritzer , C. E. , & Djang , W. T. ( 1992 ). Quantitative cerebral anatomy of the aging human brain: A cross-sectional study using magnetic resonance imaging . Neuropsychology , 42 , 527 – 536 .
   Google Scholar
• Convit , A. , de Leon , M. J. , Hoptman , M. J. , Tarshish , C. , De Santi , S. , & Rusinek , H. ( 1995 ). Age-related changes in brain: I. Magnetic resonance imaging measures of temporal lobe volumes in normal subjects . Psychiatry Quarterly , 66 , 343 – 355 .
   PubMedGoogle Scholar
• Doty , R. L. , Shaman , P. , Applebaum , S. L. , Giberson , R. , Siksorski , L. , & Rosenberg , L. ( 1984 ). Smell identification ability: Changes with age . Science , 226 , 1441 – 1443 .
   PubMed Web of Science ®Google Scholar
• Driscoll , I. , Hamilton , D. A. , Petropoulos , H. , Yeo , R. A. , Brooks , W. M. , Baumgartner , R. N. , & Sutherland , R. J. ( 2003 ). The aging hippocampus: Cognitive, biochemical and structural findings . Cerebral Cortex , 13 , 1344 – 1351 .
   PubMed Web of Science ®Google Scholar
• Dunlosky , J. & Hertzog , C. ( 1998 ). Aging and deficits in associative memory: What is the role of strategy production? Psychology and Aging , 13 , 597 – 607 .
   PubMed Web of Science ®Google Scholar
• Düzel , E. , Habib , R. , Rotte , M. , Guderian , S. , Tulving , E. , & Heinze , H. J. ( 2003 ). Human hippocampal and parahippocampal activity during visual associative recognition memory for spatial and nonspatial stimulus configurations . Journal of Neuroscience , 23 , 9439 – 9444 .
   PubMed Web of Science ®Google Scholar
• Eichenbaum , H. ( 2000 ). A cortical-hippocampal system for declarative memory . Nature Reviews Neuroscience , 1 , 41 – 50 .
   PubMed Web of Science ®Google Scholar
• Ekman , G. , Berglund , B. , Berglund , U. , & Lindvall , T. (1967). Perceived intensity of odor as a function of time of adaptation. Scandinavian Journal of Psychology , 8, 177–186.
   PubMed Web of Science ®Google Scholar
• Ferdon , S. & Murphy , C. ( 2003 ). The cerebellum and olfaction in the aging brain: A functional magnetic resonance imaging study . Neuroimage , 20 , 12 – 21 .
   PubMed Web of Science ®Google Scholar
• Fisk , J. E. & Warr , P. B. ( 1998 ). Associative learning and short-term forgetting as a function of age, perceptual speed, and central executive functioning . Journal of Gerontology , 53 , P112 – P121 .
   Google Scholar
• Folstein , M. F. , Folstein , S. E. , & McHugh , P. R. ( 1975 ). “Mini-Mental State”: A practical method for grading the cognitive state of patients for the clinician . Journal of Psychiatric Research , 12 , 189 – 198 .
   PubMed Web of Science ®Google Scholar
• Fowler , K. S. , Saling , M. M. , Conway , E. L. , Semple , J. M. , & Louis , W. J. ( 2002 ). Paired associate performance in the early detection of DAT . Journal of the International Neuropsychological Society , 8 , 58 – 71 .
   PubMed Web of Science ®Google Scholar
• Gaffan , D. ( 1994 ). Scene-specific memory for objects: A model of episodic memory impairment in monkeys with fornix transection . Journal of Cognitive Neuroscience , 6 , 305 – 320 .
   PubMed Web of Science ®Google Scholar
• Gilbert , P. E. & Kesner , R. P. ( 2002 ). Role of the rodent hippocampus in paired-associate learning involving associations between a stimulus and a spatial location . Behavioral Neuroscience , 116 , 63 – 71 .
   PubMedGoogle Scholar
• Gilbert , P. E. & Kesner , R. P. ( 2003 ). Localization of function within the dorsal hippocampus: The role of the CA3 subregion in paired-associate learning . Behavioral Neuroscience , 117 , 1385 – 1394 .
   PubMedGoogle Scholar
• Gilbert , P. E. & Kesner , R. P. ( 2004 ). Memory for objects and their locations: The role of the hippocampus in retention of object-place associations . Neurobiology of Learning and Memory , 81 , 39 – 45 .
   PubMedGoogle Scholar
• Gilbert , P. E. , Pirogovsky , E. , Ferdon , S. , & Murphy , C. ( 2006 ). The effects of normal aging on source memory for odors . The Journals of Gerontology B: Psychological Sciences and Social Sciences , 61B , P58 – P60 .
   Google Scholar
• Hamilton , J. M. , Murphy , C. , & Paulsen , J. S. ( 1999 ). Odor detection, learning, and memory in Huntington's disease . Journal of the International Neuropsychological Society , 5 , 609 – 615 .
   PubMedGoogle Scholar
• Henke , K. , Weber , B. , Kneifel , S. , Wieser , H. G. , & Buck , A. ( 1999 ). Human hippocampus associates information in memory . Proceedings of the National Academy of Sciences of the United States of America , 96 , 5884 – 5889 .
   PubMed Web of Science ®Google Scholar
• Hertzog , C. , Dunlosky , J. , Powell-Moman , A. , & Kidder , D. P. ( 2002 ). Aging and monitoring associative learning: Is monitoring accuracy spared or impaired? Psychology and Aging , 17 , 209 – 225 .
   PubMed Web of Science ®Google Scholar
• Jehl , C. & Murphy , C. ( 1998 ). Developmental effects on odor learning and memory in children . Annals of the New York Academy of Science , 855 , 632 – 634 .
   PubMedGoogle Scholar
• Jernigan , T. L. , Archibald , S. L. , Berhow , M. T. , Sowell , E. R. , Foster , D. S. , & Hesselink , J. R. ( 1991 ). Cerebral structure on MRI, Part I: Localization of age-related changes . Biological Psychiatry , 29 , 55 – 67 .
   PubMed Web of Science ®Google Scholar
• Jernigan , T. L. , Archibald , S. L. , Fennema-Notestine , C. , Gamst , A. C. , Stout , J. C. , Bonner , J. , & Hesselink , J. R. ( 2001 ). Effects of age on tissues and regions of the cerebrum and cerebellum . Neurobiology of Aging , 22 , 581 – 594 .
   PubMed Web of Science ®Google Scholar
• Jones , N. & Rog , D. (1998). Olfaction: A review. Journal of Laryngology and Otology , 112, 11–24.
   PubMedGoogle Scholar
• Kareken , D. A. , Mosnik , D. M. , Doty , R. L. , Dzemidzic , M. , & Hutchins , G. D. ( 2003 ). Functional anatomy of human odor sensation, discrimination, and identification in health and aging . Neuropsychology , 17 , 482 – 495 .
   PubMedGoogle Scholar
• Kesner , R. P. , Gilbert , P. E. , Wallenstein , G. V. ( 2000 ). Testing neural network models of memory with behavioral experiments . Current Opinions in Neurobiology , 10 , 260 – 265 .
   PubMed Web of Science ®Google Scholar
• Kesner , R. P. , Lee , I. , & Gilbert , P. E. ( 2004 ). A behavioral description of hippocampal function based on a subregional analysis . Reviews in the Neurosciences , 15 , 333 – 351 .
   PubMed Web of Science ®Google Scholar
• Kessels , R. P. , Boekhorst , S. T. , & Postma , A. ( 2005 ). The contribution of implicit and explicit memory to the effects of errorless learning: A comparison between young and older adults . Journal of the International Neuropsychological Society , 11 , 144 – 151 .
   PubMed Web of Science ®Google Scholar
• King , J. A. , Burgess , N. , Hartley , T. , Vargha-Khadem , F. , & O'Keefe , J. ( 2002 ). Human hippocampus and viewpoint dependence in spatial memory . Hippocampus , 12 , 811 – 820 .
   PubMed Web of Science ®Google Scholar
• Larsson , M. & Backman , L. ( 1993 ). Semantic activation and episodic odor recognition in young and older subjects . Psychology and Aging , 8 , 582 – 588 .
   PubMed Web of Science ®Google Scholar
• Law , J. R. , Flanery , M. A. , Wirth , S. , Yanike , M. , Smith , A. C. , Frank , L. M. , et al. ( 2005 ). Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory . Journal of Neuroscience , 25 , 5720 – 5729 .
   PubMed Web of Science ®Google Scholar
• Lemay , M. & Proteau , L. ( 2003 ). Aging affects pointing to unseen targets encoded in an allocentric frame of reference . Experimental Aging Research , 29 , 319 – 333 .
   PubMed Web of Science ®Google Scholar
• Levy , D. A. , Manns , J. R. , Hopkins , R. O. , Gold , J. J. , & Squire , L. R. ( 2003 ). Impaired visual and odor recognition memory span in patients with hippocampal lesions . Learning and Memory , 10 , 531 – 536 .
   PubMed Web of Science ®Google Scholar
• Light , L. L. , Patterson , M. M. , Chung , C. , & Healy , M. R. ( 2004 ). Effects of repetition and response deadline on associative recognition in young and older adults . Memory and Cognition , 32 , 1182 – 1193 .
   PubMed Web of Science ®Google Scholar
• Macmillan , N. A. & Creelman , D. C. ( 1991 ). Signal detection theory: A user's guide . New York : Cambridge University Press .
   Google Scholar
• Maquire , E. A. , Frith , C. , Burgess , N. , Donnett , J. , & O'Keefe , J. ( 1998 ). Knowing where things are: Parahippocampal involvement in encoding object locations in a virtual large scale space . Journal of Cognitive Neuroscience , 10 , 61 – 76 .
   PubMedGoogle Scholar
• Maguire , E. A. , Valentine , E. R. , Wilding , J. M. , & Kapur , N. ( 2003 ). Routes to remembering: The brains behind superior memory . Nature Neuroscience , 6 , 90 – 95 .
   PubMed Web of Science ®Google Scholar
• Mattis , S. ( 1976 ). Mental status examination for organic mental syndrome in the elderly patient . In L. Bellack & T. B. Katsau (Eds.), Geriatric psychiatry: A handbook for psychiatrists and primary care physicians (pp. 77 – 121 ). New York : Grune & Stratton .
   Google Scholar
• Mishkin , M. & Pribram , K. ( 1956 ). Analysis of the effects of frontal lesions in monkeys: Variations in delayed response . Journal of Comparative and Physiological Psychology , 49 , 36 – 40 .
   PubMedGoogle Scholar
• Moffat , S. D. , Zonderman , A. B. , & Resnick , S. M. (2001). Age differences in spatial memory in a virtual environment navigation task. Neurobiology of Aging , 22, 787–796.
   PubMed Web of Science ®Google Scholar
• Muller , N. G. & Knight , R. T. ( 2002 ). Age-related changes in fronto-parietal networks during spatial memory: An ERP study . Brain Research: Cognitive Brain Research , 13 , 221 – 234 .
   PubMedGoogle Scholar
• Murphy , C. , Cain , W. S. , Gilmore , M. M. , & Skinner , R. B. ( 1991 ). Sensory and semantic factors in recognition memory for odors and graphic stimuli: Elderly versus young persons . American Journal of Psychology , 104 , 161 – 192 .
   PubMed Web of Science ®Google Scholar
• Murphy , C. , Nordin , S. , & Acosta , L. ( 1997 ). Odor learning, recall, and recognition memory in young and elderly adults . Neuropsychology , 11 , 126 – 137 .
   PubMed Web of Science ®Google Scholar
• Murphy , C. , Schubert , C. R. , Cruickshanks , K. J. , Klein , B. E. , Klein , R. , & Nondahl , D. M. , ( 2002 ). Prevalence of olfactory impairment in older adults . Journal of the American Medical Association , 288 , 2307 – 2312 .
   PubMed Web of Science ®Google Scholar
• Naveh-Benjamin , M. , Guez , J. , Kilb , A. , & Reedy , S. ( 2004 ). The associative memory deficit of older adults: Further support using face-name associations . Psychology and Aging , 19 , 541 – 546 .
   PubMed Web of Science ®Google Scholar
• Nordin , S. & Murphy , C. ( 1998 ). Odor memory in normal aging and Alzheimer's disease . Annals of the New York Academy of Sciences , 855 , 686 – 693 .
   PubMed Web of Science ®Google Scholar
• Owen , A. M. , Sahakian , B. J. , Semple , J. , Polkey , E. , et al. ( 1995 ). Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man . Neuropsychologia , 33 , 1 – 24 .
   PubMed Web of Science ®Google Scholar
• Parkinson , J. K. , Murray , E. A. , & Mishkin , M. ( 1988 ). A selective mnemonic role for the hippocampus in monkeys: Memory for the location of objects . Journal of Neuroscience , 8 , 4059 – 4167 .
   Google Scholar
• Price , J. L. , Davis , P. F. , Morris , J. C. , & White , D. L. ( 1991 ). The distribution of tangles, plaques and related immunohistochemical markers in early aging and Alzheimer's disease . Neurobiology of Aging , 12 , 295 – 312 .
   PubMed Web of Science ®Google Scholar
• Rawson , N. E. , Gomez , G. , Cowart , B. , & Restrepo , D. ( 1998 ). The use of olfactory receptor neurons (ORNs) from biopsies to study changes in aging and neurodegenerative disease . Annals of the New York Academy of Sciences , 855 , 701 – 707 .
   PubMed Web of Science ®Google Scholar
• Raz , N. , Gunning , F. M. , Head , D. , Dupuis , J. H. , McQuain , J. , Briggs , S. D. , Loken , W. J. , Thornton , A. E. , & Acker , J. D. ( 1997 ). Selective aging of the human cerebral cortex observed in vivo: Differential vulnerability of the prefrontal gray matter . Cerebral Cortex , 7 , 268 – 282 .
   PubMed Web of Science ®Google Scholar
• Rodrigue , K. M. & Raz , N. ( 2004 ). Shrinkage of the entorhinal cortex over five years predicts memory performance in healthy adults . Journal of Neuroscience , 24 , 956 – 963 .
   PubMed Web of Science ®Google Scholar
• Salthouse , T. A. ( 1994 ). Aging associations: Influence of speed on adult age differences in associative learning . Journal of Experimental Psychology: Learning, Memory, and Cognition , 20 , 1486 – 1503 .
   PubMed Web of Science ®Google Scholar
• Schiffman , S. S. ( 1993 ). Perception of taste and smell in elderly persons . Critical Reviews in Food Science and Nutrition , 33 , 17 – 26 .
   PubMed Web of Science ®Google Scholar
• Schiffman , S. & Pasternak , M. ( 1979 ). Decreased discrimination of food odors in the elderly . Journals of Gerontology , 34 , 73 – 79 .
   PubMedGoogle Scholar
• Shimamura , A. P. & Squire , L. R. (1984). Paired associate learning and priming effects in amnesia: A neuropsychological study. Journal of Experimental Psychology: General , 113, 556–570.
   PubMed Web of Science ®Google Scholar
• Smith , C. G. ( 1941 ). Incidence of atrophy of the olfactory nerves in man . Archives of Otolaryngology , 34 , 33 – 539 .
   Google Scholar
• Sommer , T. , Rose , M. , Glascher , J. , Wolbers , T. , & Buchel , C. ( 2005 ). Dissociable contributions within the medial temporal lobe to encoding of object-location associations . Learning and Memory , 12 , 343 – 351 .
   PubMed Web of Science ®Google Scholar
• Squire , L. R. & Zola-Morgan , S. ( 1991 ). The medial temporal lobe memory system . Science , 253 , 1380 – 1386 .
   PubMed Web of Science ®Google Scholar
• Stark , C. E. & Squire , L. R. ( 2003 ). Hippocampal damage equally impairs memory for single items and memory for conjunctions . Hippocampus , 13 , 281 – 292 .
   PubMed Web of Science ®Google Scholar
• Stark , C. E. , Bayley , P. J. , Squire , L. R. ( 2002 ). Recognition memory for single items and for associations is similarly impaired following damage to the hippocampal region . Learning and Memory , 9 , 238 – 242 .
   PubMed Web of Science ®Google Scholar
• Stark , C. E. & Squire , L. R. ( 2001 ). Simple and associative recognition memory in the hippocampal region . Learning and Memory , 8 , 190 – 197 .
   PubMed Web of Science ®Google Scholar
• Sullivan , E. V. , Marsh , L. , Mathalon , D. H. , Lim , K. O. , & Pfefferbaum , A. ( 1995 ). Age-related decline in MRI volumes of temporal lobe gray matter but not hippocampus . Neurobiology of Aging , 16 , 591 – 606 .
   PubMed Web of Science ®Google Scholar
• Sziklas , V. & Petrides , M. ( 1999 ). The effects of lesions to the anterior thalamic nuclei on object-place associations in rats . European Journal of Neuroscience , 11 , 559 – 566 .
   PubMed Web of Science ®Google Scholar
• Warrington , E. K. & Weiskrantz , L. ( 1982 ). Amnesia: A disconnection syndrome? Neuropsychologia , 20 , 233 – 248 .
   PubMed Web of Science ®Google Scholar
• Wysocki , C. J. & Gilbert , A. ( 1989 ). National geographic smell survey: Effects of age are heterogeneous . Annals of the New York Academy of Sciences , 561 , 12 – 28 .
   PubMed Web of Science ®Google Scholar
• Yousem , D. M. , Maldjian , J. A. , Hummel , T. , Alsop , D. , Geckle , R. J. , Kraut , M. A. , & Doty , R. L. ( 1999 ). The effect of age on odor-stimulated functional MR imaging . American Journal of Neuroradiology , 20 , 600 – 608 .
   PubMedGoogle Scholar
• Zeineh , M. M. , Engel , S. A. , Thompson , P. M. , & Bookheimer , S. Y. ( 2003 ). Dynamics of the hippocampus during encoding and retrieval of face-name pairs . Science , 299 , 577 – 580 .
   PubMed Web of Science ®Google Scholar