Neural representation of navigational relevance is rapidly induced and long lasting.

Successful navigation is facilitated by the presence of landmarks. Previous functional magnetic resonance imaging (fMRI) evidence indicated that the human parahippocampal gyrus automatically distinguishes between landmarks placed at navigationally relevant (decision points) and irrelevant locations (nondecision points). This storage of navigational relevance can provide a neural mechanism underlying successful navigation. However, an efficient wayfinding mechanism requires that important spatial information is learned quickly and maintained over time. The present study investigates whether the representation of navigational relevance is modulated by time and practice. Participants learned 2 film sequences through virtual mazes containing objects at decision and at nondecision points. One maze was shown one time, and the other maze was shown 3 times. Twenty-four hours after study, event-related fMRI data were acquired during recognition of the objects. The results showed that activity in the parahippocampal gyrus was increased for objects previously placed at decision points as compared with objects placed at nondecision points. The decision point effect was not modulated by the number of exposures to the mazes and independent of explicit memory functions. These findings suggest a persistent representation of navigationally relevant information, which is stable after only one exposure to an environment. These rapidly induced and long-lasting changes in object representation provide a basis for successful wayfinding.

[1]  N. Kanwisher,et al.  Visual attention: Insights from brain imaging , 2000, Nature Reviews Neuroscience.

[2]  Mark D'Esposito,et al.  A functional MRI study of the influence of practice on component processes of working memory , 2004, NeuroImage.

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

[4]  D. Amaral,et al.  Memory and the Hippocampus , 1989 .

[5]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[6]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[7]  E. Maguire,et al.  Knowing Where Things Are: Parahippocampal Involvement in Encoding Object Locations in Virtual Large-Scale Space , 1998, Journal of Cognitive Neuroscience.

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

[9]  J. Gabrieli,et al.  Neural Correlates of Encoding Space from Route and Survey Perspectives , 2002, The Journal of Neuroscience.

[10]  Pierre Maquet,et al.  Brain activity underlying encoding and retrieval of source memory. , 2002, Cerebral cortex.

[11]  L. Squire,et al.  Simple and associative recognition memory in the hippocampal region. , 2001, Learning & memory.

[12]  M. D’Esposito,et al.  The parahippocampus subserves topographical learning in man , 1996, NeuroImage.

[13]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[14]  Hans-Jochen Heinze,et al.  Human Hippocampal and Parahippocampal Activity during Visual Associative Recognition Memory for Spatial and Nonspatial Stimulus Configurations , 2003, The Journal of Neuroscience.

[15]  M. Chun,et al.  Attentional Modulation of Learning-Related Repetition Attenuation Effects in Human Parahippocampal Cortex , 2005, The Journal of Neuroscience.

[16]  C. Degueldre,et al.  Are Spatial Memories Strengthened in the Human Hippocampus during Slow Wave Sleep? , 2004, Neuron.

[17]  Daniel L. Schacter,et al.  Brain regions associated with retrieval of structurally coherent visual information , 1995, Nature.

[18]  Alex Martin,et al.  Modulation of neural activity during object naming: effects of time and practice. , 2003, Cerebral cortex.

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

[20]  P Alvarez,et al.  Memory consolidation and the medial temporal lobe: a simple network model. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

[22]  R. Henson.  A Mini-Review of fMRI Studies of Human Medial Temporal Lobe Activity Associated with Recognition Memory , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

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

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

[25]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[26]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[27]  G. Winocur,et al.  “I have often walked down this street before”: fMRI Studies on the hippocampus and other structures during mental navigation of an old environment , 2004, Hippocampus.

[28]  Raymond J. Dolan,et al.  Selective Attention Modulates Neural Substrates of Repetition Priming and Implicit Visual Memory: Suppressions and Enhancements Revealed by fMRI , 2005, Journal of Cognitive Neuroscience.

[29]  Paul E. Downing,et al.  Viewpoint-Specific Scene Representations in Human Parahippocampal Cortex , 2003, Neuron.

[30]  Pierre Maquet,et al.  Sleep and brain plasticity , 2003 .

[31]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

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

[33]  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.

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

[35]  Gabriele Janzen,et al.  Selective neural representation of objects relevant for navigation , 2004, Nature Neuroscience.

[36]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[37]  Russell A. Epstein,et al.  The Parahippocampal Place Area Recognition, Navigation, or Encoding? , 1999, Neuron.

[38]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[39]  T. Klingberg,et al.  Increased prefrontal and parietal activity after training of working memory , 2004, Nature Neuroscience.

[40]  Sharon L. Thompson-Schill,et al.  Learning Places from Views: Variation in Scene Processing as a Function of Experience and Navigational Ability , 2005, Journal of Cognitive Neuroscience.