Virtual environment navigation tasks and the assessment of cognitive deficits in individuals with brain injury

Navigation in real environments is often impaired by traumatic brain injury (TBI). These deficits in wayfinding appear to be due to disruption of cognitive processes underlying navigation and may in turn be due to damage to the hippocampus and frontal lobes. These wayfinding problems after TBI were investigated using a virtual simulation of a Morris Water Maze (MWM), a standard test of hippocampal function in laboratory animals. The virtual environment consisted of a large virtual arena in a very large virtual room whose walls provided views of a naturalistic landscape. Eleven community-dwelling TBI survivors and 12 comparison participants, matched for gender, age and education were tested to see if they could find a location in the arena marked by one of the following: (a) a visible platform, (b) a single proximal object, (c) a single proximal object among seven other distracter objects, or (d) distal features inside and outside the room. The proximal objects allowed participants to use egocentric (body-centered) navigational strategies that rely on relatively simple stimulus-response associations. The absence of proximal cues forced the participants to rely on distal features of the environment (room walls, landscape elements) and tested their ability to use allocentric (world-based) navigational strategies requiring cognitive mapping. Results indicated that the navigation of TBI survivors was not impaired when the proximal cues were present but was impaired when proximal cues were absent. These results provide more evidence that the navigational deficit after TBI is due to an inability to form, remember or use cognitive maps.

[1]  John J. B. Allen,et al.  Memory Deficits Characterized by Patterns of Lesions to the Hippocampus and Parahippocampal Cortex , 2000, Annals of the New York Academy of Sciences.

[2]  J. Barrash.  A historical review of topographical disorientation and its neuroanatomical correlates. , 1998, Journal of clinical and experimental neuropsychology.

[3]  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.

[4]  R. J. McDonald,et al.  Multiple Parallel Memory Systems in the Brain of the Rat , 2002, Neurobiology of Learning and Memory.

[5]  Sterling C. Johnson,et al.  Traumatic brain injury and memory: The role of hippocampal atrophy. , 1996 .

[6]  D F Tate,et al.  Fornix and hippocampal atrophy in traumatic brain injury. , 2000, Learning & memory.

[7]  Hanna Damasio,et al.  The neuroanatomical correlates of route learning impairment , 2000, Neuropsychologia.

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

[9]  Cindy M. Bukach,et al.  Humans With Traumatic Brain Injuries Show Place-Learning Deficits in Computer-Generated Virtual Space , 2000, Journal of clinical and experimental neuropsychology.

[10]  K. Jeffery,et al.  The Hippocampal and Parietal Foundations of Spatial Cognition , 1999 .

[11]  J. Feigenbaum,et al.  Deficits in spatial working memory after unilateral temporal lobectomy in man , 1996, Neuropsychologia.

[12]  Fary Khan,et al.  4: Rehabilitation after traumatic brain injury , 2003, The Medical journal of Australia.

[13]  Paul Green,et al.  The lesion(s) in traumatic brain injury: implications for clinical neuropsychology. , 2003, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[14]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[15]  B. Brooks.  Route learning in a case of amnesia : A preliminary investigation into the efficacy of training in a virtual environment , 1999 .

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

[17]  I. Whishaw,et al.  Sequential control of navigation by locale and taxon cues in the Morris water task , 2004, Behavioural Brain Research.

[18]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[19]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[20]  Klaus P. Ebmeier,et al.  Memory impairment in out-of-hospital cardiac arrest survivors is associated with global reduction in brain volume, not focal hippocampal injury. , 2000, Stroke.

[21]  Giuseppe Iaria,et al.  Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. , 2004, Neuropsychology.

[22]  J. Cronly-Dillon,et al.  Visual Agnosias and Other Disturbances of Visual Perception and Cognition , 1991 .

[23]  R. Sutherland,et al.  A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. , 1983, Behavioral neuroscience.

[24]  J. Stiles-Davis,et al.  Spatial cognition : brain bases and development , 1988 .

[25]  Lynn Nadel,et al.  The spatial brain. , 2004, Neuropsychology.

[26]  L. Nerad,et al.  Human spatial navigation deficits after traumatic brain injury shown in the arena maze, a virtual Morris water maze , 2006, Brain injury.

[27]  B. Kolb,et al.  Behavioural and anatomical studies of the posterior parietal cortex in the rat , 1987, Behavioural Brain Research.

[28]  T. I. King,et al.  Introduction to Cognitive Rehabilitation: Theory and Practice , 1991 .

[29]  R. Reitan,et al.  A selective and critical review of neuropsychological deficits and the frontal lobes , 1994, Neuropsychology Review.

[30]  E. Tolman.  Cognitive maps in rats and men. , 1948, Psychological review.

[31]  Neil Burgess,et al.  Integrating hippocampal and parietal functions: a spatial point of view , 1998 .

[32]  Albert A. Rizzo,et al.  Analysis of assets for virtual reality applications in neuropsychology , 2004 .

[33]  J. Barrash,et al.  Age‐related decline in route learning ability , 1994 .

[34]  Barbara A. Wilson,et al.  Towards a comprehensive model of cognitive rehabilitation , 2002 .

[35]  Assessment of the behavioral consequences of head trauma , 1989 .

[36]  M. Rappaport,et al.  Head injury outcome up to ten years later. , 1989, Archives of physical medicine and rehabilitation.

[37]  O. L. Zangwill,et al.  DISORDERS OF VISUAL SPACE PERCEPTION ASSOCIATED WITH LESIONS OF THE RIGHT CEREBRAL HEMISPHERE , 1944 .

[38]  A. Sirigu,et al.  Pure Topographical Disorientation: A Definition and Anatomical Basis , 1987, Cortex.

[39]  J. Alvarez,et al.  Executive Function and the Frontal Lobes: A Meta-Analytic Review , 2006, Neuropsychology Review.

[40]  O. Spreen,et al.  A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary , 1991 .

[41]  R. Skelton.  Modelling recovery of cognitive function after traumatic brain injury: spatial navigation in the Morris water maze after complete or partial transections of the perforant path in rats , 1998, Behavioural Brain Research.

[42]  Brenda Milner,et al.  The role of the right hippocampus in the recall of spatial location , 1981, Neuropsychologia.

[43]  R. Morris.  Developments of a water-maze procedure for studying spatial learning in the rat , 1984, Journal of Neuroscience Methods.

[44]  H. Eichenbaum,et al.  Hippocampal representation in place learning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  E. Bigler,et al.  Hippocampal volume in normal aging and traumatic brain injury. , 1997, AJNR. American journal of neuroradiology.

[46]  J. Grafman,et al.  Clock Drawing in Alzheimer's Disease , 1989, Journal of the American Geriatrics Society.

[47]  Lucia F Jacobs,et al.  Unpacking the cognitive map: the parallel map theory of hippocampal function. , 2003, Psychological review.

[48]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[49]  A. V. Zomeren,et al.  Residual complaints of patients two years after severe head injury. , 1985 .

[50]  H. Scharfman,et al.  The parahippocampal region. Implications for neurological and psychiatric diseases. Introduction. , 2000, Annals of the New York Academy of Sciences.

[51]  N Burgess,et al.  Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. , 2001, Brain : a journal of neurology.

[52]  G. Wolf-Klein,et al.  Screening for Alzheimer's Disease by Clock Drawing , 1989, Journal of the American Geriatrics Society.

[53]  J. Adams,et al.  Hippocampal pathology in fatal non-missile human head injury , 2004, Acta Neuropathologica.

[54]  E. Maguire,et al.  Topographical disorientation following unilateral temporal lobe lesions in humans , 1996, Neuropsychologia.

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

[56]  R. Morris.  Spatial Localization Does Not Require the Presence of Local Cues , 1981 .

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