Individual Differences in Human Path Integration Abilities Correlate with Gray Matter Volume in Retrosplenial Cortex, Hippocampus, and Medial Prefrontal Cortex

Abstract Humans differ in their individual navigational abilities. These individual differences may exist in part because successful navigation relies on several disparate abilities, which rely on different brain structures. One such navigational capability is path integration, the updating of position and orientation, in which navigators track distances, directions, and locations in space during movement. Although structural differences related to landmark-based navigation have been examined, gray matter volume related to path integration ability has not yet been tested. Here, we examined individual differences in two path integration paradigms: (1) a location tracking task and (2) a task tracking translational and rotational self-motion. Using voxel-based morphometry, we related differences in performance in these path integration tasks to variation in brain morphology in 26 healthy young adults. Performance in the location tracking task positively correlated with individual differences in gray matter volume in three areas critical for path integration: the hippocampus, the retrosplenial cortex, and the medial prefrontal cortex. These regions are consistent with the path integration system known from computational and animal models and provide novel evidence that morphological variability in retrosplenial and medial prefrontal cortices underlies individual differences in human path integration ability. The results for tracking rotational self-motion—but not translation or location—demonstrated that cerebellum gray matter volume correlated with individual performance. Our findings also suggest that these three aspects of path integration are largely independent. Together, the results of this study provide a link between individual abilities and the functional correlates, computational models, and animal models of path integration.

[1]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[2]  M. Moser,et al.  Impaired Spatial Representation in CA1 after Lesion of Direct Input from Entorhinal Cortex , 2008, Neuron.

[3]  Adam M. P. Miller,et al.  Cues, context, and long-term memory: the role of the retrosplenial cortex in spatial cognition , 2014, Front. Hum. Neurosci..

[4]  Russell A. Epstein Parahippocampal and retrosplenial contributions to human spatial navigation , 2008, Trends in Cognitive Sciences.

[5]  J. Aggleton Looking beyond the hippocampus: old and new neurological targets for understanding memory disorders , 2014, Proceedings of the Royal Society B: Biological Sciences.

[6]  R. Klatzky,et al.  Nonvisual navigation by blind and sighted: assessment of path integration ability. , 1993, Journal of experimental psychology. General.

[7]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[8]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[9]  E. Maguire,et al.  Acquiring “the Knowledge” of London's Layout Drives Structural Brain Changes , 2011, Current Biology.

[10]  C. A. Rovira Acquiring knowledge , 1990 .

[11]  Karl J. Friston,et al.  Voxel-based morphometry of the human brain: Methods and applications , 2005 .

[12]  E. Save,et al.  Dissociation of the effects of bilateral lesions of the dorsal hippocampus and parietal cortex on path integration in the rat. , 2001, Behavioral neuroscience.

[13]  A. Berthoz,et al.  Dissociable cognitive mechanisms underlying human path integration , 2010, Experimental Brain Research.

[14]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[15]  Christian F. Doeller,et al.  Anterior Hippocampus and Goal-Directed Spatial Decision Making , 2011, The Journal of Neuroscience.

[16]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Roberta L. Klatzky,et al.  Human navigation ability: Tests of the encoding-error model of path integration , 1999, Spatial Cogn. Comput..

[18]  N. Ramnani The primate cortico-cerebellar system: anatomy and function , 2006, Nature Reviews Neuroscience.

[19]  Catherine J. Stoodley,et al.  The Cerebellum and Cognition: Evidence from Functional Imaging Studies , 2011, The Cerebellum.

[20]  R Wehner,et al.  Path integration in desert ants, Cataglyphis fortis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Aiden E. G. F. Arnold,et al.  Differential neural network configuration during human path integration , 2014, Front. Hum. Neurosci..

[22]  M. Behrmann,et al.  Path Integration Deficits during Linear Locomotion after Human Medial Temporal Lobectomy , 2004, Journal of Cognitive Neuroscience.

[23]  Simon Benhamou,et al.  Spatial memory in large scale movements: Efficiency and limitation of the egocentric coding process , 1990 .

[24]  M. Hegarty,et al.  A dissociation between object manipulation spatial ability and spatial orientation ability , 2001, Memory & cognition.

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

[26]  Reginald G. Golledge,et al.  A Minimal Representation for Dead-Reckoning Navigation: Updating the Homing Vector , 2010 .

[27]  J. Money,et al.  Turner's syndrome: further demonstration of the presence of specific cognitional deficiencies. , 1966, Journal of medical genetics.

[28]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[29]  T. Hartley,et al.  An association between human hippocampal volume and topographical memory in healthy young adults , 2012, Front. Hum. Neurosci..

[30]  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.

[31]  E. Save,et al.  Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[33]  E. Maguire,et al.  London taxi drivers and bus drivers: A structural MRI and neuropsychological analysis , 2006, Hippocampus.

[34]  Bruno Poucet,et al.  Role of the parietal cortex in long-term representation of spatial information in the rat , 2009, Neurobiology of Learning and Memory.

[35]  Russell A. Epstein,et al.  Distances between Real-World Locations Are Represented in the Human Hippocampus , 2011, The Journal of Neuroscience.

[36]  H. Spiers,et al.  Path integration following temporal lobectomy in humans , 2001, Neuropsychologia.

[37]  Russell A. Epstein,et al.  Anchoring the neural compass: Coding of local spatial reference frames in human medial parietal lobe , 2014, Nature Neuroscience.

[38]  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.

[39]  Jeremy D. Schmahmann,et al.  Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study , 2012, NeuroImage.

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

[41]  E. McAuley,et al.  Exercise training increases size of hippocampus and improves memory , 2011, Proceedings of the National Academy of Sciences.

[42]  Véronique D. Bohbot,et al.  Spatial navigational strategies correlate with gray matter in the hippocampus of healthy older adults tested in a virtual maze , 2013, Front. Ag. Neurosci..

[43]  M. Hasselmo,et al.  Persistence of Parahippocampal Representation in the Absence of Stimulus Input Enhances Long-Term Encoding: A Functional Magnetic Resonance Imaging Study of Subsequent Memory after a Delayed Match-to-Sample Task , 2004, The Journal of Neuroscience.

[44]  Daniel A. Gajewski,et al.  Medial Temporal Lobe Roles in Human Path Integration , 2014, PloS one.

[45]  Elizabeth R. Chrastil,et al.  Which way and how far? Tracking of translation and rotation information for human path integration , 2016, Human brain mapping.

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

[47]  Giuseppe Iaria,et al.  Gray Matter Differences Correlate with Spontaneous Strategies in a Human Virtual Navigation Task , 2007, The Journal of Neuroscience.

[48]  J. O’Keefe,et al.  An oscillatory interference model of grid cell firing , 2007, Hippocampus.

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

[50]  M. Hasselmo A model of episodic memory: Mental time travel along encoded trajectories using grid cells , 2009, Neurobiology of Learning and Memory.

[51]  G. Schlaug,et al.  Brain Structures Differ between Musicians and Non-Musicians , 2003, The Journal of Neuroscience.

[52]  Chantal E Stern,et al.  Contributions of the hippocampal subfields and entorhinal cortex to disambiguation during working memory , 2013, Hippocampus.

[53]  R. Knight,et al.  The Hippocampus and Entorhinal Cortex Encode the Path and Euclidean Distances to Goals during Navigation , 2014, Current Biology.

[54]  Arne D. Ekstrom,et al.  Human neural systems underlying rigid and flexible forms of allocentric spatial representation , 2013, Human brain mapping.

[55]  Tianzi Jiang,et al.  Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures , 2012, NeuroImage.

[56]  H. Eichenbaum,et al.  Interplay of Hippocampus and Prefrontal Cortex in Memory , 2013, Current Biology.

[57]  Russell A. Epstein,et al.  Hippocampal size predicts rapid learning of a cognitive map in humans , 2013, Hippocampus.

[58]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[59]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

[60]  Katherine R. Sherrill,et al.  Hippocampus and Retrosplenial Cortex Combine Path Integration Signals for Successful Navigation , 2013, The Journal of Neuroscience.

[61]  Elizabeth R. Chrastil,et al.  Neural evidence supports a novel framework for spatial navigation , 2012, Psychonomic Bulletin & Review.

[62]  Alan C. Evans,et al.  Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space , 1999, NeuroImage.

[63]  Irem Aselcioglu,et al.  Structural Differences in Hippocampal and Prefrontal Gray Matter Volume Support Flexible Context-Dependent Navigation Ability , 2014, The Journal of Neuroscience.

[64]  H. Damasio Human Brain Anatomy in Computerized Images , 1995 .

[65]  Giuseppe Iaria,et al.  Navigational skills correlate with hippocampal fractional anisotropy in humans , 2008, Hippocampus.

[66]  Christian F. Doeller,et al.  Interaction Between Hippocampus and Cerebellum Crus I in Sequence-Based but not Place-Based Navigation. , 2015, Cerebral cortex.

[67]  C. Büchel,et al.  Differential Recruitment of the Hippocampus, Medial Prefrontal Cortex, and the Human Motion Complex during Path Integration in Humans , 2007, The Journal of Neuroscience.

[68]  Elizabeth R. Chrastil,et al.  There and Back Again: Hippocampus and Retrosplenial Cortex Track Homing Distance during Human Path Integration , 2015, The Journal of Neuroscience.

[69]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[70]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.

[71]  Gabriele Janzen,et al.  Gray and white matter correlates of navigational ability in humans , 2014, Human brain mapping.

[72]  Barbara Tversky,et al.  Mental spatial transformations of objects and perspective , 2001, Spatial Cogn. Comput..

[73]  Anthony E. Richardson,et al.  Development of a self-report measure of environmental spatial ability. , 2002 .

[74]  Alan C. Evans,et al.  Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. , 2000, Cerebral cortex.

[75]  Hugo J Spiers,et al.  A navigational guidance system in the human brain , 2007, Hippocampus.

[76]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[77]  C. Gallistel The organization of learning , 1990 .

[78]  Mary Hegarty,et al.  What determines our navigational abilities? , 2010, Trends in Cognitive Sciences.

[79]  D. Simons,et al.  Striatal volume predicts level of video game skill acquisition. , 2010, Cerebral cortex.

[80]  Reginald G. Golledge,et al.  The Encoding-Error Model of Pathway Completion without Vision , 2010 .

[81]  Shawn S. Winter,et al.  The medial frontal cortex contributes to but does not organize rat exploratory behavior , 2016, Neuroscience.

[82]  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.

[83]  Ian Q Whishaw,et al.  Hippocampal lesions and path integration , 1997, Current Opinion in Neurobiology.

[84]  N. Takahashi,et al.  Pure topographic disorientation due to right retrosplenial lesion , 1997, Neurology.

[85]  P. E. Sharp,et al.  Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. , 2001, Behavioral neuroscience.

[86]  M. Moser,et al.  A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation , 2015, Nature.

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

[88]  Jason B. Mattingley,et al.  Medial Parietal Cortex Encodes Perceived Heading Direction in Humans , 2010, The Journal of Neuroscience.

[89]  Alan C. Evans,et al.  Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. , 2002, Cerebral cortex.

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

[91]  Marko Pfeifer Human Brain Anatomy In Computerized Images , 2016 .

[92]  Uğur M Erdem,et al.  A goal‐directed spatial navigation model using forward trajectory planning based on grid cells , 2012, The European journal of neuroscience.