When memory does not fail: familiarity-based recognition in mild cognitive impairment and Alzheimer's disease.

Recognition can be guided by familiarity, a restricted form of retrieval devoid of contextual recall, or by recollection, which occurs when retrieval is sufficient to support the full experience of remembering an episode. Recollection and familiarity were disentangled by testing recognition memory using silhouette object drawings, high target-foil resemblance, and both yes-no and forced-choice procedures. Theoretically, forced-choice recognition could be mediated by familiarity alone. Alzheimer's disease and its preclinical stage, mild cognitive impairment (MCI), were associated with memory impairments that were greater on the yes-no test. Remarkably, forced-choice recognition was unequivocally normal in patients with MCI compared with age-matched controls. Neuropathology in hippocampus and entorhinal cortex, known to be present in MCI, presumably disrupted recollection while leaving familiarity-based recognition intact.

[1]  M H Buonocore,et al.  Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study , 2001, Neuroreport.

[2]  Andrew P. Yonelinas,et al.  Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology , 2005, Neuropsychologia.

[3]  R. K. Simpson.  Nature Neuroscience , 2022 .

[4]  B. Leonard,et al.  Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  J. Morris,et al.  The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assesment of Alzheimer's disease , 1989, Neurology.

[6]  R Ratcliff,et al.  Testing global memory models using ROC curves. , 1992, Psychological review.

[7]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[8]  Robert T Knight,et al.  The contribution of recollection and familiarity to yes–no and forced-choice recognition tests in healthy subjects and amnesics , 2000, Neuropsychologia.

[9]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[10]  J. Morris,et al.  Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease , 1996, The Journal of Neuroscience.

[11]  Christine Bastin,et al.  The contribution of recollection and familiarity to recognition memory: a study of the effects of test format and aging. , 2003, Neuropsychology.

[12]  G. Barba,et al.  Recognition Memory and Recollective Experience in Alzheimer's Disease , 1997 .

[13]  Joseph R. Manns,et al.  Recognition Memory and the Human Hippocampus , 2003, Neuron.

[14]  J. Morris,et al.  Current concepts in mild cognitive impairment. , 2001, Archives of neurology.

[15]  C. Jack,et al.  Mild cognitive impairment – beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment , 2004, Journal of internal medicine.

[16]  R. O’Reilly,et al.  Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. , 2003, Psychological review.

[17]  E. Salmon,et al.  Controlled and automatic memory processes in Alzheimer’s disease , 2000 .

[18]  D. Schacter,et al.  Associative recognition in Alzheimer's disease: evidence for impaired recall-to-reject. , 2004, Neuropsychology.

[19]  Seth J. Ramus,et al.  Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system , 1994, Hippocampus.

[20]  Suzanne Corkin,et al.  Visual dysfunction in Alzheimer's disease: Relation to normal aging , 1991, Annals of neurology.

[21]  Anthony F Jorm.  A short form of the Informant Questionnaire on Cognitive Decline in the Elderly (IQCODE): development and cross-validation , 1994, Psychological Medicine.

[22]  L R Squire,et al.  Remembering and knowing: two different expressions of declarative memory. , 1995, Journal of experimental psychology. Learning, memory, and cognition.

[23]  M. W. Brown,et al.  Recognition memory: neuronal substrates of the judgement of prior occurrence , 1998, Progress in Neurobiology.

[24]  J. Morris.  The Clinical Dementia Rating (CDR) , 1993, Neurology.

[25]  R. Morris.  The cognitive neuropsychology of Alzheimer-type dementia , 1996 .

[26]  E. Kaplan,et al.  The Boston naming test , 2001 .

[27]  David G. Amaral,et al.  Introduction: What is where in the medial temporal lobe? , 1999, Hippocampus.

[28]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[29]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

[30]  Mortimer Mishkin,et al.  Preserved Recognition in a Case of Developmental Amnesia: Implications for the Acaquisition of Semantic Memory? , 2001, Journal of Cognitive Neuroscience.

[31]  Ken A Paller,et al.  The neural basis of the butcher-on-the-bus phenomenon: when a face seems familiar but is not remembered , 2004, NeuroImage.

[32]  C. Kawas,et al.  Neuropathology in controls and demented subjects from the Baltimore longitudinal study of aging , 1996, Neurobiology of Aging.

[33]  M. Albert,et al.  Temporal lobe regions on magnetic resonance imaging identify patients with early Alzheimer's disease. , 1993, Archives of neurology.

[34]  W. Jagust,et al.  Regional cerebral glucose transport and utilization in Alzheimer's disease , 1989, Neurology.

[35]  D L Schacter,et al.  When false recognition is unopposed by true recognition: gist-based memory distortion in Alzheimer's disease. , 2000, Neuropsychology.

[36]  John M. Gardiner,et al.  Experiences of Remembering, Knowing, and Guessing , 1998, Consciousness and Cognition.

[37]  Robert T. Knight,et al.  Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity , 2002, Nature Neuroscience.

[38]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[39]  S. Leurgans,et al.  MRI predictors of risk of incident Alzheimer disease , 2005, Neurology.

[40]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease , 1984, Neurology.

[41]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[42]  A. Yonelinas.  The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[43]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[44]  Dc Washington.  Diagnostic and Statistical Manual of Mental Disorders, 4th Ed. , 1994 .

[45]  L. Mansi,et al.  CORTICAL ABNORMALITIES IN ALZHEIMER'S DISEASE , 1984, Annals of neurology.

[46]  E. Tulving.  Memory and consciousness. , 1985 .

[47]  D. Schacter,et al.  The cognitive neuroscience of constructive memory. , 1998, Annual review of psychology.

[48]  G. Mandler.  Recognizing: The judgment of previous occurrence. , 1980 .

[49]  P. Lachenbruch.  Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[50]  Giovanni B. Frisoni,et al.  Distinctive Clinical Features of Mild Cognitive Impairment with Subcortical Cerebrovascular Disease , 2005, Dementia and Geriatric Cognitive Disorders.

[51]  J. Touchon,et al.  Disability and mild cognitive impairment: a longitudinal population‐based study , 2001, International journal of geriatric psychiatry.

[52]  M. Mesulam.  Neuroplasticity Failure in Alzheimer's Disease Bridging the Gap between Plaques and Tangles , 1999, Neuron.

[53]  D. Loewenstein,et al.  Mild cognitive impairment , 2003, Neurology.

[54]  C. Jack,et al.  Usefulness of MRI measures of entorhinal cortex versus hippocampus in AD , 2000, Neurology.

[55]  W. Jagust,et al.  Quantitative NMR measurements of hippocampal atrophy in Alzheimer's disease , 1988, Magnetic resonance in medicine.

[56]  A. Delacourte,et al.  The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer’s disease , 1999, Neurology.

[57]  A P Yonelinas,et al.  The contribution of recollection and familiarity to recognition and source-memory judgments: a formal dual-process model and an analysis of receiver operating characteristics. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[58]  S. Black,et al.  Memory impairments associated with hippocampal versus parahippocampal-gyrus atrophy: an MR volumetry study in Alzheimer’s disease , 1998, Neuropsychologia.

[59]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[60]  R. Reitan.  Trail Making Test: Manual for Administration and Scoring , 1992 .

[61]  M. Mesulam,et al.  Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive impairment. , 2003, Archives of neurology.

[62]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[63]  M. Linden,et al.  Dissociation Between Recall and Recognition Memory Performance in an Amnesic Patient with Hippocampal Damage Following Carbon Monoxide Poisoning , 2004, Neurocase.

[64]  N. Schuff,et al.  Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease , 2001, Journal of neurology, neurosurgery, and psychiatry.

[65]  B. A. Keys,et al.  Varying patterns of verbal recall, recognition, and response bias with progression of alzheimer's disease. , 1997, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[66]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[67]  H. Soininen,et al.  Volumes of the Entorhinal and Perirhinal Cortices in Alzheimer’s Disease , 1998, Neurobiology of Aging.

[68]  A. Yonelinas.  Receiver-operating characteristics in recognition memory: evidence for a dual-process model. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[69]  G. Alexander,et al.  Regional glucose metabolic abnormalities are not the result of atrophy in Alzheimer's disease , 1998, Neurology.

[70]  J. Troncoso,et al.  Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease , 1994, The Lancet.

[71]  B Horwitz,et al.  Longitudinal study of the early neuropsychological and cerebral metabolic changes in dementia of the Alzheimer type. , 1988, Journal of clinical and experimental neuropsychology.

[72]  M. Mesulam,et al.  Cholinergic nucleus basalis tauopathy emerges early in the aging‐MCI‐AD continuum , 2004, Annals of neurology.

[73]  J. Morris,et al.  Tangles and plaques in nondemented aging and “preclinical” Alzheimer's disease , 1999, Annals of neurology.

[74]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[76]  V. Reyna,et al.  Fuzzy-trace theory: An interim synthesis , 1995 .

[77]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[78]  D. Bennett,et al.  Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment , 2001, Annals of neurology.

[79]  Y. Stern,et al.  Functional deficits in patients with mild cognitive impairment: Prediction of AD , 2002, Neurology.

[80]  M. Koivisto,et al.  Automatic Influences of Memory in Alzheimer's Disease , 1998, Cortex.

[81]  B. Reisberg,et al.  Positron emission tomographic studies of aging and Alzheimer disease. , 1983, AJNR. American journal of neuroradiology.

[82]  R. O’Reilly,et al.  Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? , 2002, Hippocampus.

[83]  Hans-Jochen Heinze,et al.  Neural correlates of recognition memory with and without recollection in patients with Alzheimer's disease and healthy controls , 1999, Neuroscience Letters.

[84]  H. Braak,et al.  Neuropathological stageing of Alzheimer-related changes , 2004, Acta Neuropathologica.

[85]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[86]  A. Richardson-Klavehn,et al.  Remembering and knowing , 2000 .

[87]  D Tsivilis,et al.  Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition , 2004, Hippocampus.

[88]  H. Soininen,et al.  Hippocampus and entorhinal cortex in mild cognitive impairment and early AD , 2004, Neurobiology of Aging.

[89]  D. Schacter,et al.  Perceptual false recognition in Alzheimer's disease. , 2001, Neuropsychology.

[90]  A. Yonelinas,et al.  Separating sensitivity from response bias: implications of comparisons of yes-no and forced-choice tests for models and measures of recognition memory. , 2002, Journal of experimental psychology. General.

[91]  R. Knight.  Controlled and Automatic Memory Process in Alzheimer's Disease , 1998, Cortex.

[92]  M. Verfaellie,et al.  The relationship between recall and recognition in amnesia: effects of matching recognition between patients with amnesia and controls. , 2001, Neuropsychology.

[93]  J. Orgogozo,et al.  Vascular cognitive disorder: a new diagnostic category updating vascular cognitive impairment and vascular dementia , 2004, Journal of the Neurological Sciences.

[94]  G Dalla Barba,et al.  Recognition memory and recollective experience in Alzheimer's disease. , 1997, Memory.

[95]  D. Schacter,et al.  False Recognition in Alzheimer Disease: Evidence from Categorized Pictures , 2003, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[96]  R. Henson,et al.  A familiarity signal in human anterior medial temporal cortex? , 2003, Hippocampus.

[97]  N. Schuff,et al.  Higher atrophy rate of entorhinal cortex than hippocampus in AD , 2004, Neurology.

[98]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[99]  N. Hunkin,et al.  Relative sparing of item recognition memory in a patient with adult‐onset damage limited to the hippocampus , 2002, Hippocampus.