Behavioral Neuroscience Mini Review Article Neural Correlates of Spatial Navigation Changes in Mild Cognitive Impairment and Alzheimer's Disease

Although the memory impairment is a hallmark of Alzheimer’s disease (AD), AD has also been characterized by spatial disorientation, which is present from its early stages. Spatial disorientation in AD manifests itself in getting lost in familiar and unfamiliar places and have been characterized more specifically using spatial navigation tests in both real space and virtual environments as an impairment in multiple spatial abilities, including allocentric and egocentric navigation strategies, visuo-spatial perception, or selection of relevant information for successful navigation. Patients suffering mild cognitive impairment (MCI), who are at a high risk of development of dementia, show impairment in a subset of these abilities, mainly connected with allocentric and egocentric processing. While spatial disorientation in typical AD patients probably reflects neurodegenerative changes in medial and posterior temporal, parietal, and frontal lobes, and retrosplenial cortex, the impairment of spatial navigation in MCI seem to be connected mainly with the medial temporal and also parietal brain changes. In this review, we will summarize the signs of brain disease in most MCI and AD patients showing in various tasks of spatial memory and navigation.

[1]  S. Becker,et al.  Remembering the past and imagining the future: a neural model of spatial memory and imagery. , 2007, Psychological review.

[2]  G. Frisoni,et al.  SPECT predictors of cognitive decline and Alzheimer's disease in mild cognitive impairment. , 2009, Journal of Alzheimer's disease : JAD.

[3]  André A Fenton,et al.  Object–location memory impairment in patients with thermal lesions to the right or left hippocampus , 2004, Neuropsychologia.

[4]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[5]  Romola S. Bucks,et al.  Development and validation of the Location Learning Test (LLT): A test of visuo-spatial learning designed for use with older adults and in dementia , 1997 .

[6]  M. D’Esposito,et al.  Topographical disorientation: a synthesis and taxonomy. , 1999, Brain : a journal of neurology.

[7]  J. Baron,et al.  Mapping gray matter loss with voxel-based morphometry in mild cognitive impairment , 2002, Neuroreport.

[8]  C. Jack,et al.  Longitudinal MRI atrophy biomarkers: Relationship to conversion in the ADNI cohort , 2010, Neurobiology of Aging.

[9]  J. Gray,et al.  Allocentric spatial memory activation of the hippocampal formation measured with fMRI. , 2004, Neuropsychology.

[10]  R. Kesner,et al.  Spatial recognition and spatial order memory in patients with dementia of the Alzheimer's type , 1992, Neuropsychologia.

[11]  N. Burgess,et al.  The hippocampus is required for short‐term topographical memory in humans , 2007, Hippocampus.

[12]  R. Passini,et al.  Wayfinding in dementia of the Alzheimer type: planning abilities. , 1995, Journal of clinical and experimental neuropsychology.

[13]  J. Feigenbaum,et al.  Allocentric versus egocentric spatial memory after unilateral temporal lobectomy in humans. , 2004, Neuropsychology.

[14]  S Minoshima,et al.  Preclinical evidence of Alzheimer changes in progressive mild cognitive impairment: a qualitative and quantitative SPECT study , 2006, Acta neurologica Scandinavica.

[15]  Eini Niskanen,et al.  Voxel-based morphometry to detect brain atrophy in progressive mild cognitive impairment , 2007, NeuroImage.

[16]  M. D’Esposito,et al.  An Area within Human Ventral Cortex Sensitive to “Building” Stimuli Evidence and Implications , 1998, Neuron.

[17]  Charles J Duffy,et al.  A visuospatial variant of mild cognitive impairment , 2003, Neurology.

[18]  M. Albert,et al.  Single photon emission computed tomography perfusion differences in mild cognitive impairment , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[19]  R. Petersen,et al.  Neuropathologically defined subtypes of Alzheimer's disease with distinct clinical characteristics: a retrospective study , 2011, The Lancet Neurology.

[20]  Laure Rondi-Reig,et al.  Temporal Order Memory Assessed during Spatiotemporal Navigation As a Behavioral Cognitive Marker for Differential Alzheimer's Disease Diagnosis , 2012, The Journal of Neuroscience.

[21]  K. Perryman,et al.  Route learning performance in Alzheimer disease patients. , 2001, Neuropsychiatry, neuropsychology, and behavioral neurology.

[22]  H. Braak,et al.  Staging of alzheimer's disease-related neurofibrillary changes , 1995, Neurobiology of Aging.

[23]  A. Dale,et al.  Relative capability of MR imaging and FDG PET to depict changes associated with prodromal and early Alzheimer disease. , 2010, Radiology.

[24]  André Dufour,et al.  Spatial navigation in normal aging and the prodromal stage of Alzheimer's disease: Insights from imaging and behavioral studies , 2013, Ageing Research Reviews.

[25]  Lars-Olof Wahlund,et al.  Cingulate cortex hypoperfusion predicts Alzheimer's disease in mild cognitive impairment , 2002, BMC neurology.

[26]  永福 智志.  The Organization of Learning , 2005, Journal of Cognitive Neuroscience.

[27]  Nick C Fox,et al.  Amnestic Mild Cognitive Impairment: Structural MR Imaging Findings Predictive of Conversion to Alzheimer Disease , 2008, American Journal of Neuroradiology.

[28]  Adam N Mamelak,et al.  Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task , 2002, Behavioural Brain Research.

[29]  Andy C. H. Lee,et al.  Specialization in the medial temporal lobe for processing of objects and scenes , 2005, Hippocampus.

[30]  A. Dale,et al.  Structural MRI biomarkers for preclinical and mild Alzheimer's disease , 2009, Human brain mapping.

[31]  E. Tangalos,et al.  Neuropathologic features of amnestic mild cognitive impairment. , 2006, Archives of neurology.

[32]  C. Duffy,et al.  Visual loss and getting lost in Alzheimer’s disease , 1999, Neurology.

[33]  R. Passini,et al.  Performances of patients with a dementia of the Alzheimer type in the Standardized Road-Map test of Direction Sense , 2002, Neuropsychologia.

[34]  G. Kemmler,et al.  Neuropsychological Deficits Associated With Route Learning in Alzheimer Disease, MCI, and Normal Aging , 2014, Alzheimer disease and associated disorders.

[35]  W Makous,et al.  Visual mechanisms of spatial disorientation in Alzheimer's disease. , 2001, Cerebral cortex.

[36]  J R Hodges,et al.  Retrosplenial cortex (BA 29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer's disease) , 2003, The European journal of neuroscience.

[37]  Charles J Duffy,et al.  Detecting navigational deficits in cognitive aging and Alzheimer disease using virtual reality , 2008, Neurology.

[38]  Vincenzo Paolo Senese,et al.  Visuospatial memory in healthy elderly, AD and MCI: a review. , 2009, Current aging science.

[39]  C. Duffy,et al.  Neurophysiological and perceptual correlates of navigational impairment in Alzheimer's disease. , 2006, Brain : a journal of neurology.

[40]  et al.,et al.  Categorical and correlational analyses of baseline fluorodeoxyglucose positron emission tomography images from the Alzheimer's Disease Neuroimaging Initiative (ADNI) , 2009, NeuroImage.

[41]  Jelle Jolles,et al.  Atrophy of the parietal lobe in preclinical dementia , 2011, Brain and Cognition.

[42]  K. Vlček,et al.  Spatial Navigation Impairment in Healthy Aging and Alzheimer’s Disease , 2011 .

[43]  J. Hodges,et al.  Limbic hypometabolism in Alzheimer's disease and mild cognitive impairment , 2003, Annals of neurology.

[44]  Christian Büchel,et al.  Neural foundations of emerging route knowledge in complex spatial environments. , 2004, Brain research. Cognitive brain research.

[45]  G. Frisoni,et al.  Brain SPECT in subtypes of mild cognitive impairment , 2008, Journal of Neurology.

[46]  N. Burgess,et al.  Lost and found: bespoke memory testing for Alzheimer's disease and semantic dementia. , 2010, Journal of Alzheimer's disease : JAD.

[47]  A. Dale,et al.  Regional rates of neocortical atrophy from normal aging to early Alzheimer disease , 2009, Neurology.

[48]  Christian Büchel,et al.  Spatial updating: how the brain keeps track of changing object locations during observer motion , 2008, Nature Neuroscience.

[49]  Nick C Fox,et al.  Mapping the evolution of regional atrophy in Alzheimer's disease: Unbiased analysis of fluid-registered serial MRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[50]  F. Schmitt,et al.  Brain structural alterations before mild cognitive impairment , 2007, Neurology.

[51]  M. Valis,et al.  Effect of Donepezil in Alzheimer Disease Can Be Measured by a Computerized Human Analog of the Morris Water Maze , 2013, Neurodegenerative Diseases.

[52]  R. Passingham.  The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[53]  A. Drzezga,et al.  Cerebral metabolic changes accompanying conversion of mild cognitive impairment into Alzheimer's disease: a PET follow-up study , 2003, European Journal of Nuclear Medicine and Molecular Imaging.

[54]  Godehard Weniger,et al.  Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment , 2011, Neuropsychologia.

[55]  Jan Bureš,et al.  Allothetic orientation and sequential ordering of places is impaired in early stages of Alzheimer's disease: corresponding results in real space tests and computer tests , 2005, Behavioural Brain Research.

[56]  Guy B. Williams,et al.  The relationship of topographical memory performance to regional neurodegeneration in Alzheimer's disease , 2012, Front. Ag. Neurosci..

[57]  S. Pappatà,et al.  SPECT imaging of GABAA/benzodiazepine receptors and cerebral perfusion in mild cognitive impairment , 2010, European Journal of Nuclear Medicine and Molecular Imaging.

[58]  Jakub Hort,et al.  Spatial navigation impairment is proportional to right hippocampal volume , 2012, Proceedings of the National Academy of Sciences.

[59]  C. Duffy,et al.  The Sex Specificity of Navigational Strategies in Alzheimer Disease , 2007, Alzheimer disease and associated disorders.

[60]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[61]  N. Burgess,et al.  Topographical short‐term memory differentiates Alzheimer's disease from frontotemporal lobar degeneration , 2009, Hippocampus.

[62]  Philip S. Insel,et al.  Nonlinear time course of brain volume loss in cognitively normal and impaired elders , 2012, Neurobiology of Aging.

[63]  Keith A. Johnson,et al.  Intelligence quotient–adjusted memory impairment is associated with abnormal single photon emission computed tomography perfusion , 2007, Journal of the International Neuropsychological Society.

[64]  G. Riva,et al.  From allo- to egocentric spatial ability in early Alzheimer’s disease: A study with virtual reality spatial tasks , 2013, Cognitive neuroscience.

[65]  J. Hodges,et al.  Focal posterior cingulate atrophy in incipient Alzheimer's disease , 2010, Neurobiology of Aging.

[66]  L. Mucke,et al.  Spatial cognition and the human navigation network in AD and MCI , 2007, Neurology.

[67]  Giuseppe Riva,et al.  Getting lost in Alzheimer's disease: a break in the mental frame syncing. , 2013, Medical hypotheses.

[68]  J. Bureš,et al.  Spatial navigation deficit in amnestic mild cognitive impairment , 2007, Proceedings of the National Academy of Sciences.

[69]  Eini Niskanen,et al.  Evolution of global and local grey matter atrophy on serial MRI scans during the progression from MCI to AD. , 2012, Current Alzheimer research.

[70]  C. Jack,et al.  MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment , 2008, Neurology.

[71]  Tobias Schmidt-Wilcke,et al.  Memory performance correlates with gray matter density in the ento-/perirhinal cortex and posterior hippocampus in patients with mild cognitive impairment and healthy controls — A voxel based morphometry study , 2009, NeuroImage.

[72]  Andy C. H. Lee,et al.  Differentiating the Roles of the Hippocampus and Perirhinal Cortex in Processes beyond Long-Term Declarative Memory: A Double Dissociation in Dementia , 2006, The Journal of Neuroscience.

[73]  Christian F. Doeller,et al.  Lateralized human hippocampal activity predicts navigation based on sequence or place memory , 2010, Proceedings of the National Academy of Sciences.

[74]  Hiroshi Matsuda,et al.  The prediction of rapid conversion to Alzheimer's disease in mild cognitive impairment using regional cerebral blood flow SPECT , 2005, NeuroImage.

[75]  M. Cherrier,et al.  Agnosia for scenes in topographagnosia , 2003, Neuropsychologia.

[76]  V. Henderson,et al.  Spatial disorientation in Alzheimer's disease. , 1989, Archives of Neurology.

[77]  R. Kessels,et al.  Categorical spatial memory in patients with mild cognitive impairment and Alzheimer dementia: Positional versus object-location recall , 2009, Journal of the International Neuropsychological Society.

[78]  Jakub Hort,et al.  Spatial navigation testing discriminates two types of amnestic mild cognitive impairment , 2009, Behavioural Brain Research.

[79]  B Milner,et al.  Right medial temporal-lobe contribution to object-location memory. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[80]  H. Rusinek,et al.  Regional analysis of FDG and PIB-PET images in normal aging, mild cognitive impairment, and Alzheimer’s disease , 2008, European Journal of Nuclear Medicine and Molecular Imaging.

[81]  C. Jack,et al.  Neuroimaging correlates of pathologically defined subtypes of Alzheimer's disease: a case-control study , 2012, The Lancet Neurology.

[82]  M. Petrides,et al.  Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice , 2003, The Journal of Neuroscience.

[83]  J. Brandt,et al.  Differential impairment of spatial location memory in Huntington’s disease , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[84]  Alan C. Evans,et al.  Cortical Thickness Analysis to Detect Progressive Mild Cognitive Impairment: A Reference to Alzheimer’s Disease , 2009, Dementia and Geriatric Cognitive Disorders.

[85]  Albert Postma,et al.  Spatial memory deficits in patients after unilateral selective amygdalohippocampectomy , 2004, Journal of the International Neuropsychological Society.

[86]  D. Burr,et al.  A cortical area that responds specifically to optic flow, revealed by fMRI , 2000, Nature Neuroscience.

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

[88]  Jakub Hort,et al.  Spatial navigation—a unique window into physiological and pathological aging , 2012, Front. Ag. Neurosci..