Which way and how far? Tracking of translation and rotation information for human path integration

Path integration, the constant updating of the navigator's knowledge of position and orientation during movement, requires both visuospatial knowledge and memory. This study aimed to develop a systems‐level understanding of human path integration by examining the basic building blocks of path integration in humans. To achieve this goal, we used functional imaging to examine the neural mechanisms that support the tracking and memory of translational and rotational components of human path integration. Critically, and in contrast to previous studies, we examined movement in translation and rotation tasks with no defined end‐point or goal. Navigators accumulated translational and rotational information during virtual self‐motion. Activity in hippocampus, retrosplenial cortex (RSC), and parahippocampal cortex (PHC) increased during both translation and rotation encoding, suggesting that these regions track self‐motion information during path integration. These results address current questions regarding distance coding in the human brain. By implementing a modified delayed match to sample paradigm, we also examined the encoding and maintenance of path integration signals in working memory. Hippocampus, PHC, and RSC were recruited during successful encoding and maintenance of path integration information, with RSC selective for tasks that required processing heading rotation changes. These data indicate distinct working memory mechanisms for translation and rotation, which are essential for updating neural representations of current location. The results provide evidence that hippocampus, PHC, and RSC flexibly track task‐relevant translation and rotation signals for path integration and could form the hub of a more distributed network supporting spatial navigation. Hum Brain Mapp 37:3636–3655, 2016. © 2016 Wiley Periodicals, Inc.

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

[2]  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.

[3]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[6]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[7]  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.

[8]  J. Hodges Memory, Amnesia and the Hippocampal System , 1995 .

[9]  J. Taube Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  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.

[11]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

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

[13]  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.

[14]  K M Gothard,et al.  Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues , 1996, The Journal of Neuroscience.

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

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

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

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

[19]  B. McNaughton,et al.  Hippocampectomized rats are capable of homing by path integration. , 1999, Behavioral neuroscience.

[20]  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.

[21]  M Behrmann,et al.  Active control of locomotion facilitates nonvisual navigation. , 2001, Journal of experimental psychology. Human perception and performance.

[22]  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.

[23]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

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

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

[26]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[27]  William H Warren,et al.  Path Integration from Optic Flow and Body Senses in a Homing Task , 2002, Perception.

[28]  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.

[29]  T. Kimura,et al.  Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus , 2002, Neuroscience Letters.

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

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

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

[35]  M. Fyhn,et al.  Spatial Representation in the Entorhinal Cortex , 2004, Science.

[36]  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.

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

[38]  Hideshi Shibata,et al.  Organization of retrosplenial cortical projections to the anterior cingulate, motor, and prefrontal cortices in the rat , 2004, Neuroscience Research.

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

[40]  M. Hasselmo,et al.  Scopolamine Reduces Persistent Activity Related to Long-Term Encoding in the Parahippocampal Gyrus during Delayed Matching in Humans , 2005, The Journal of Neuroscience.

[41]  Michael X. Cohen,et al.  Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence , 2005, Journal of Cognitive Neuroscience.

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

[43]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

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

[45]  Torkel Hafting,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006, Science.

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

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

[48]  J. O'Doherty,et al.  Model‐Based fMRI and Its Application to Reward Learning and Decision Making , 2007, Annals of the New York Academy of Sciences.

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

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

[51]  M. Bar,et al.  The parahippocampal cortex mediates spatial and nonspatial associations. , 2007, Cerebral cortex.

[52]  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.

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

[54]  Adam Johnson,et al.  Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point , 2007, The Journal of Neuroscience.

[55]  A. Treves,et al.  Hippocampal remapping and grid realignment in entorhinal cortex , 2007, Nature.

[56]  Cornelis G. Weststeijn,et al.  Neural representation of object location and route direction: An event-related fMRI study , 2007, Brain Research.

[57]  Larry R Squire,et al.  Neural basis of the cognitive map: Path integration does not require hippocampus or entorhinal cortex , 2008, Proceedings of the National Academy of Sciences.

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

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

[60]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

[61]  John C. Rothwell,et al.  Posterior parietal rTMS disrupts human Path Integration during a vestibular navigation task , 2008, Neuroscience Letters.

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

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

[64]  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.

[65]  Christian F. Doeller,et al.  Evidence for grid cells in a human memory network , 2010, Nature.

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

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

[68]  Thackery I. Brown,et al.  Which Way Was I Going? Contextual Retrieval Supports the Disambiguation of Well Learned Overlapping Navigational Routes , 2010, The Journal of Neuroscience.

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

[70]  Alain Berthoz,et al.  Multiple reference frames used by the human brain for spatial perception and memory , 2010, Experimental Brain Research.

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

[72]  Michael J Kahana,et al.  A sense of direction in human entorhinal cortex , 2010, Proceedings of the National Academy of Sciences.

[73]  H. Eichenbaum,et al.  Hippocampal “Time Cells” Bridge the Gap in Memory for Discontiguous Events , 2011, Neuron.

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

[75]  Joseph T. McGuire,et al.  A Neural Signature of Hierarchical Reinforcement Learning , 2011, Neuron.

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

[77]  Menno Witter,et al.  The Retrosplenial Cortex: Intrinsic Connectivity and Connections with the (Para)Hippocampal Region in the Rat. An Interactive Connectome , 2011, Front. Neuroinform..

[78]  Dylan A. Simon,et al.  Neural Correlates of Forward Planning in a Spatial Decision Task in Humans , 2011, The Journal of Neuroscience.

[79]  Neil Burgess,et al.  Visual influence on path integration in darkness indicates a multimodal representation of large-scale space , 2011, Proceedings of the National Academy of Sciences.

[80]  Steven A. Marchette,et al.  Cognitive Mappers to Creatures of Habit: Differential Engagement of Place and Response Learning Mechanisms Predicts Human Navigational Behavior , 2011, The Journal of Neuroscience.

[81]  R. Saunders,et al.  Medial Temporal Lobe Projections to the Retrosplenial Cortex of the Macaque Monkey , 2012, Hippocampus.

[82]  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.

[83]  Chantal E. Stern,et al.  Cooperative interactions between hippocampal and striatal systems support flexible navigation , 2012, NeuroImage.

[84]  Brad E. Pfeiffer,et al.  Hippocampal place cell sequences depict future paths to remembered goals , 2013, Nature.

[85]  Armin Brandt,et al.  Neural Activity in Human Hippocampal Formation Reveals the Spatial Context of Retrieved Memories , 2013, Science.

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

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

[88]  Russell A. Epstein,et al.  Abstract Representations of Location and Facing Direction in the Human Brain , 2013, The Journal of Neuroscience.

[89]  Benjamin J. Kraus,et al.  Hippocampal “Time Cells”: Time versus Path Integration , 2013, Neuron.

[90]  Larry R Squire,et al.  Contrasting effects on path integration after hippocampal damage in humans and rats , 2013, Proceedings of the National Academy of Sciences.

[91]  I. Fried,et al.  Direct recordings of grid-like neuronal activity in human spatial navigation , 2013, Nature Neuroscience.

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

[93]  Xiao-Jing Wang,et al.  The importance of mixed selectivity in complex cognitive tasks , 2013, Nature.

[94]  B. P. Klein,et al.  Topographic Representation of Numerosity in the Human Parietal Cortex , 2013, Science.

[95]  Blake S. Porter,et al.  Hippocampal Representation of Related and Opposing Memories Develop within Distinct, Hierarchically Organized Neural Schemas , 2014, Neuron.

[96]  Gui Xue,et al.  Global Neural Pattern Similarity as a Common Basis for Categorization and Recognition Memory , 2014, The Journal of Neuroscience.

[97]  Thackery I. Brown,et al.  A High‐resolution study of hippocampal and medial temporal lobe correlates of spatial context and prospective overlapping route memory , 2014, Hippocampus.

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

[99]  Matthew T. Kaufman,et al.  A category-free neural population supports evolving demands during decision-making , 2014, Nature Neuroscience.

[100]  Elizabeth R. Chrastil,et al.  Does the human odometer use an extrinsic or intrinsic metric? , 2013, Attention, Perception, & Psychophysics.

[101]  Russell A. Epstein,et al.  Neural systems for landmark-based wayfinding in humans , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[102]  Neal J. Cohen,et al.  The role of the hippocampus in flexible cognition and social behavior , 2014, Front. Hum. Neurosci..

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

[104]  Aiden E. G. F. Arnold,et al.  A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective , 2014, Front. Hum. Neurosci..

[105]  Anjali Krishnan,et al.  Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations , 2014, NeuroImage.

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

[107]  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..

[108]  Thackery I. Brown,et al.  Contributions of medial temporal lobe and striatal memory systems to learning and retrieving overlapping spatial memories. , 2014, Cerebral cortex.

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

[110]  N. Burgess,et al.  The Cognitive Architecture of Spatial Navigation: Hippocampal and Striatal Contributions , 2015, Neuron.

[111]  S. Dumoulin,et al.  Transformation from a Retinal to a Cyclopean Representation in Human Visual Cortex , 2015, Current Biology.

[112]  Andrew S. Whiteman,et al.  Hippocampal subfield and medial temporal cortical persistent activity during working memory reflects ongoing encoding , 2015, Front. Syst. Neurosci..

[113]  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.

[114]  B. J. Clark,et al.  Passive Transport Disrupts Grid Signals in the Parahippocampal Cortex , 2015, Current Biology.

[115]  Caswell Barry,et al.  Neural systems supporting navigation , 2015, Current Opinion in Behavioral Sciences.

[116]  Stefano Fusi,et al.  Why neurons mix: high dimensionality for higher cognition , 2016, Current Opinion in Neurobiology.

[117]  Arne D. Ekstrom,et al.  Oscillations Go the Distance: Low-Frequency Human Hippocampal Oscillations Code Spatial Distance in the Absence of Sensory Cues during Teleportation , 2016, Neuron.

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