Maladaptive Bias for Extrahippocampal Navigation Strategies in Aging Humans

Efficient spatial navigation requires not only accurate spatial knowledge but also the selection of appropriate strategies. Using a novel paradigm that allowed us to distinguish between beacon, associative cue, and place strategies, we investigated the effects of cognitive aging on the selection and adoption of navigation strategies in humans. Participants were required to rejoin a previously learned route encountered from an unfamiliar direction. Successful performance required the use of an allocentric place strategy, which was increasingly observed in young participants over six experimental sessions. In contrast, older participants, who were able to recall the route when approaching intersections from the same direction as during encoding, failed to use the correct place strategy when approaching intersections from novel directions. Instead, they continuously used a beacon strategy and showed no evidence of changing their behavior across the six sessions. Given that this bias was already apparent in the first experimental session, the inability to adopt the correct place strategy is not related to an inability to switch from a firmly established response strategy to an allocentric place strategy. Rather, and in line with previous research, age-related deficits in allocentric processing result in shifts in preferred navigation strategies and an overall bias for response strategies. The specific preference for a beacon strategy is discussed in the context of a possible dissociation between beacon-based and associative-cue-based response learning in the striatum, with the latter being more sensitive to age-related changes.

[1]  N. Raz,et al.  Extrahippocampal contributions to age differences in human spatial navigation. , 2007, Cerebral cortex.

[2]  B. Knowlton,et al.  Contributions of striatal subregions to place and response learning. , 2004, Learning & memory.

[3]  P. Lipman,et al.  Age and exposure differences in acquisition of route information. , 1991, Psychology and aging.

[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]  N. Burgess.  Spatial Cognition and the Brain , 2008, Annals of the New York Academy of Sciences.

[6]  Christian F. Doeller,et al.  Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory , 2008, Proceedings of the National Academy of Sciences.

[7]  J. Bizon,et al.  Emergence of a cue strategy preference on the water maze task in aged C57B6 x SJL F1 hybrid mice. , 2003, Learning & memory.

[8]  C. Büchel,et al.  Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations , 2005, The Journal of Neuroscience.

[9]  R. J. McDonald,et al.  Lesions of the dorsolateral striatum impair the acquisition of a simplified stimulus-response dependent conditional discrimination task , 2005, Neuroscience.

[10]  R. J. McDonald,et al.  Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. , 1994, Behavioral and neural biology.

[11]  S. Resnick,et al.  Effects of age on virtual environment place navigation and allocentric cognitive mapping. , 2002, Behavioral neuroscience.

[12]  N. White,et al.  Parallel Information Processing in the Dorsal Striatum: Relation to Hippocampal Function , 1999, The Journal of Neuroscience.

[13]  A Begega,et al.  Effects of ageing on allocentric and egocentric spatial strategies in the Wistar rat , 2001, Behavioural Processes.

[14]  S. Haber.  The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[15]  K. Nakano,et al.  Neural circuits and functional organization of the striatum , 2000, Journal of Neurology.

[16]  J. D. McGaugh,et al.  Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning , 1996, Neurobiology of Learning and Memory.

[17]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[18]  B. Balleine,et al.  Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action , 2010, Neuropsychopharmacology.

[19]  Y. Lippa,et al.  Landmarks as beacons and associative cues: Their role in route learning , 2007, Memory & cognition.

[20]  D. Head,et al.  Age effects on wayfinding and route learning skills , 2010, Behavioural Brain Research.

[21]  T. Robbins,et al.  Putting a spin on the dorsal–ventral divide of the striatum , 2004, Trends in Neurosciences.

[22]  Thomas Wolbers,et al.  Ageing effects on path integration and landmark navigation , 2012, Hippocampus.

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

[24]  Jari Tiihonen,et al.  Different effect of age on dopamine transporters in the dorsal and ventral striatum of controls and alcoholics , 2003, Synapse.

[25]  Gabriele Janzen,et al.  Landmark Recognition in Alzheimer’s Dementia: Spared Implicit Memory for Objects Relevant for Navigation , 2011, PloS one.

[26]  Zang-Hee Cho,et al.  Effects of age on dopamine D2 receptor availability in striatal subdivisions: A high-resolution positron emission tomography study , 2011, European Neuropsychopharmacology.

[27]  S. Moffat,et al.  Effects of age on navigation strategy , 2012, Neurobiology of Aging.

[28]  J. Wiener,et al.  Route repetition and route retracing: effects of cognitive aging , 2012, Front. Ag. Neurosci..

[29]  M. Mattson,et al.  Selective Vulnerability of Neurons in Layer II of the Entorhinal Cortex during Aging and Alzheimer's Disease , 2010, Neural plasticity.

[30]  R. J. McDonald,et al.  Dorsal striatum and stimulus–response learning: lesions of the dorsolateral, but not dorsomedial, striatum impair acquisition of a simple discrimination task , 2004, Behavioural Brain Research.

[31]  C. Luis,et al.  Cross validation of the Montreal Cognitive Assessment in community dwelling older adults residing in the Southeastern US , 2009, International journal of geriatric psychiatry.

[32]  U. Lindenberger,et al.  Adult age differences in task switching. , 2000, Psychology and aging.

[33]  H. Brody,et al.  The aging brain , 1992, Acta neurologica Scandinavica. Supplementum.

[34]  J. Cummings,et al.  The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment , 2005, Journal of the American Geriatrics Society.

[35]  F. Herrmann.  34 Cognitive reserve and survival , 2012, Neurobiology of Aging.

[36]  John A. King,et al.  Human hippocampus and viewpoint dependence in spatial memory , 2002, Hippocampus.

[37]  Carol A Barnes,et al.  Neurobiological changes in the hippocampus during normative aging. , 2009, Archives of neurology.

[38]  Guillén Fernández,et al.  Interaction between the Human Hippocampus and the Caudate Nucleus during Route Recognition , 2004, Neuron.

[39]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[40]  J. Barton,et al.  Age differences in the formation and use of cognitive maps , 2009, Behavioural Brain Research.

[41]  R. Skelton,et al.  Spatial deficits in a virtual water maze in amnesic participants with hippocampal damage , 2009, Hippocampus.