Attentional dynamics and visual perception: mechanisms of spatial disorientation in Alzheimer's disease.

Visuospatial disorientation forces Alzheimer's disease patients to abandon independent activities. We found previously that limitations of ambulatory and vehicular navigation are linked to impaired visual motion processing in Alzheimer's disease. We now hypothesize that these perceptual impairments reflect temporal constraints on visual attention. We evaluated attentional, perceptual and neuropsychological capacities in 14 Alzheimer's disease patients and 12 age-matched older normal controls. The temporal dynamics of visual attention were measured using rapid serial visual presentation (RSVP) to assess the attentional blink. Visual processing for spatial orientation was assessed using perceptual thresholds for optic flow, the visual motion seen during observer self-movement. Alzheimer's disease patients show an exaggerated attentional blink during RSVP, identifying the first of two targets but missing the second target depending on the number of intervening distractors. They also show a unique form of attentional masking in which they miss the first target but identify the second, again depending on the number of intervening distractors. Both types of RSVP errors are correlated with selectively elevated optic flow thresholds in Alzheimer's disease patients. This suggests that temporal constraints on visual perception might impair optic flow analysis and contribute to spatial disorientation in Alzheimer's disease. These findings are consistent with two-stage models of visual perception, suggesting that the working memory mechanisms in the second stage provide feedback control of input to category-specific perceptual processors in the first stage.

[1]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[2]  H. Eichenbaum,et al.  The Hippocampus and Disambiguation of Overlapping Sequences , 2002, The Journal of Neuroscience.

[3]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[4]  Charles J. Duffy,et al.  Cortical Neurons Encoding Path and Place: Where You Go Is Where You Are , 2002, Science.

[5]  Christian Keysers,et al.  Visual masking and RSVP reveal neural competition , 2002, Trends in Cognitive Sciences.

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

[7]  J. Raymond.  Perceptual links and attentional blinks , 2001 .

[8]  K. Shapiro.  Temporal methods for studying attention: how did we get here and where are we going? , 2001 .

[9]  James T. Enns,et al.  Visual masking and task switching in the attentional blink , 2001 .

[10]  K. Shapiro.  The limits of attention : temporal constraints in human information processing , 2001 .

[11]  Ravi S. Menon,et al.  Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. , 2001, Journal of neurophysiology.

[12]  M. Rizzo,et al.  Increased attentional blink after focal cerebral lesions , 2001, Neurology.

[13]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

[14]  H. Karnath.  New insights into the functions of the superior temporal cortex , 2001, Nature Reviews Neuroscience.

[15]  G. A. Orban,et al.  Human Brain Regions Involved in Heading Estimation , 2001, The Journal of Neuroscience.

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

[17]  Jeffrey L. Cummings,et al.  Cognitive and behavioral heterogeneity in Alzheimer’s disease: seeking the neurobiological basis , 2000, Neurobiology of Aging.

[18]  J. Gore,et al.  Neural Correlates of the Attentional Blink , 2000, Neuron.

[19]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

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

[21]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[22]  W S Maki,et al.  Sources of the attentional blink during rapid serial visual presentation: perceptual interference and retrieval competition. , 1997, Journal of experimental psychology. Human perception and performance.

[23]  Robert H. Wurtz,et al.  Multiple temporal components of optic flow responses in MST neurons , 1997, Experimental Brain Research.

[24]  M. D’Esposito,et al.  Environmental Knowledge Is Subserved by Separable Dorsal/Ventral Neural Areas , 1997, The Journal of Neuroscience.

[25]  C. Kennard,et al.  Abnormal temporal dynamics of visual attention in spatial neglect patients , 1997, Nature.

[26]  K Cheng,et al.  Human cortical regions activated by wide-field visual motion: an H2(15)O PET study. , 1995, Journal of neurophysiology.

[27]  A. Dale,et al.  Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging , 1995, Nature.

[28]  M. Potter,et al.  A two-stage model for multiple target detection in rapid serial visual presentation. , 1995, Journal of experimental psychology. Human perception and performance.

[29]  S. Feldon,et al.  Dissociation between the detection and perception of motion in Alzheimer's disease , 1994, Neurology.

[30]  G. Orban,et al.  Many areas in the human brain respond to visual motion. , 1994, Journal of neurophysiology.

[31]  H. Bülthoff,et al.  Separate neural pathways for the visual analysis of object shape in perception and prehension , 1994, Current Biology.

[32]  Cheryl L. Grady,et al.  Functional Associations among Human Posterior Extrastriate Brain Regions during Object and Spatial Vision , 1992, Journal of Cognitive Neuroscience.

[33]  N Butters,et al.  Directed and divided attention in Alzheimer's disease: impairment in shifting of attention to global and local stimuli. , 1992, Journal of clinical and experimental neuropsychology.

[34]  N Mai,et al.  Disturbance of movement vision after bilateral posterior brain damage. Further evidence and follow up observations. , 1991, Brain : a journal of neurology.

[35]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[37]  D. Broadbent,et al.  From detection to identification: Response to multiple targets in rapid serial visual presentation , 1987, Perception & psychophysics.

[38]  Lewis O. Harvey,et al.  Efficient estimation of sensory thresholds , 1986 .

[39]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[40]  M. Moscovitch,et al.  Visual processing deficits as assessed by spatial frequency contrast sensitivity and backward masking in normal ageing and Alzheimer's disease. , 1984, Brain : a journal of neurology.

[41]  M. Eckardt.  The Hippocampus as a Cognitive Map , 1980 .

[42]  S. Folstein,et al.  “Mini-mental state”: A practical method for grading the cognitive state of patients for the clinician , 1975 .

[43]  G. Holmes.  DISTURBANCES OF VISION BY CEREBRAL LESIONS , 1918, The British journal of ophthalmology.

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

[45]  D. N. Pandya,et al.  Further observations on parieto-temporal connections in the rhesus monkey , 2004, Experimental Brain Research.

[46]  V. Coltheart.  Fleeting memories : cognition of brief visual stimuli , 1999 .

[47]  Raja Parasuraman,et al.  Selective attention in aging and dementia. , 1998 .

[48]  R. Parasuraman.  The attentive brain , 1998 .

[49]  W E Skaggs,et al.  Deciphering the hippocampal polyglot: the hippocampus as a path integration system. , 1996, The Journal of experimental biology.

[50]  Karen M. Arnell,et al.  Attention to visual pattern information produces the attentional blink in rapid serial visual presentation. , 1994, Journal of experimental psychology. Human perception and performance.

[51]  K L Shapiro,et al.  Temporary suppression of visual processing in an RSVP task: an attentional blink? . , 1992, Journal of experimental psychology. Human perception and performance.

[52]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[53]  Leslie G. Ungerleider.  Two cortical visual systems , 1982 .

[54]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[55]  J. Money,et al.  A standardized road-map test of direction sense , 1965 .

[56]  W. Taylor.  Attention and perception. , 1954 .

[57]  M. Critchleey.  [Parietal lobes]. , 1953, Giornale di psichiatria e di neuropatologia.

[58]  E. Boring.  The perception of the visual world. , 1951 .