Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation

Recent computational models suggest that visual input from optic flow provides information about egocentric (navigator-centered) motion and influences firing patterns in spatially tuned cells during navigation. Computationally, self-motion cues can be extracted from optic flow during navigation. Despite the importance of optic flow to navigation, a functional link between brain regions sensitive to optic flow and brain regions important for navigation has not been established in either humans or animals. Here, we used a beta-series correlation methodology coupled with two fMRI tasks to establish this functional link during goal-directed navigation in humans. Functionally defined optic flow sensitive cortical areas V3A, V6, and hMT+ were used as seed regions. fMRI data was collected during a navigation task in which participants updated position and orientation based on self-motion cues to successfully navigate to an encoded goal location. The results demonstrate that goal-directed navigation requiring updating of position and orientation in the first person perspective involves a cooperative interaction between optic flow sensitive regions V3A, V6, and hMT+ and the hippocampus, retrosplenial cortex, posterior parietal cortex, and medial prefrontal cortex. These functional connections suggest a dynamic interaction between these systems to support goal-directed navigation.

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

[2]  M. Schölvinck,et al.  Neural basis of global resting-state fMRI activity , 2010, Proceedings of the National Academy of Sciences.

[3]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[4]  Ravi S. Menon,et al.  Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. , 2001, Journal of neurophysiology.

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

[6]  Adam Gazzaley,et al.  Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. , 2007, Cerebral cortex.

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

[8]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[9]  S. Mizumori,et al.  Temporary Inactivation of the Retrosplenial Cortex Causes a Transient Reorganization of Spatial Coding in the Hippocampus , 2001, The Journal of Neuroscience.

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

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

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

[13]  Michael E. Hasselmo,et al.  Modeling Boundary Vector Cell Firing Given Optic Flow as a Cue , 2012, PLoS Comput. Biol..

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

[15]  R L Klatzky,et al.  Path integration while ignoring irrelevant movement. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[16]  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.

[17]  Andrew P. Duchon,et al.  Do Humans Integrate Routes Into a Cognitive Map? Map- Versus Landmark-Based Navigation of Novel Shortcuts , 2005 .

[18]  Charles J Duffy,et al.  Visual Motion Processing in Aging and Alzheimer's Disease , 2009, Annals of the New York Academy of Sciences.

[19]  Hideo Sakata,et al.  Navigation-associated medial parietal neurons in monkeys , 2006, Proceedings of the National Academy of Sciences.

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

[21]  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.

[22]  Andrew D. Straw,et al.  Vision Egg: an Open-Source Library for Realtime Visual Stimulus Generation , 2008, Frontiers Neuroinformatics.

[23]  Etienne Save,et al.  The retrosplenial cortex is necessary for path integration in the dark , 2014, Behavioural Brain Research.

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

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

[26]  Velia Cardin,et al.  Sensitivity of human visual cortical area V6 to stereoscopic depth gradients associated with self-motion , 2011, Journal of neurophysiology.

[27]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

[28]  Andreas Bartels,et al.  Human Areas V3A and V6 Compensate for Self-Induced Planar Visual Motion , 2012, Neuron.

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

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

[31]  Chantal E Stern,et al.  The retrieval of learned sequences engages the hippocampus: Evidence from fMRI , 2009, Hippocampus.

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

[33]  Seralynne D Vann,et al.  Do rats with retrosplenial cortex lesions lack direction? , 2008, The European journal of neuroscience.

[34]  C. Galletti,et al.  Wide-Field Retinotopy Defines Human Cortical Visual Area V6 , 2006, The Journal of Neuroscience.

[35]  Michael E. Hasselmo,et al.  Modeling the influence of optic flow on grid cell firing in the absence of other cues1 , 2012, Journal of Computational Neuroscience.

[36]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[37]  J. O’Keefe,et al.  Modeling place fields in terms of the cortical inputs to the hippocampus , 2000, Hippocampus.

[38]  Eleanor A. Maguire,et al.  Thoughts, behaviour, and brain dynamics during navigation in the real world , 2006, NeuroImage.

[39]  David J Logan,et al.  Cerebral Cortex doi:10.1093/cercor/bhj082 Cerebral Cortex Advance Access published December 7, 2005 Cortical Area MSTd Combines Visual Cues , 2022 .

[40]  C. Galletti,et al.  Human V6: The Medial Motion Area , 2009, Cerebral cortex.

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

[42]  Lotfi B Merabet,et al.  Visual Topography of Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[43]  Markus Lappe,et al.  Visual selectivity for heading in monkey area MST , 2009, Experimental Brain Research.

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

[45]  Cameron S Carter,et al.  Cognitive Control Deficits in Schizophrenia: Mechanisms and Meaning , 2011, Neuropsychopharmacology.

[46]  G. A. Orban,et al.  Human Brain Regions Involved in Heading Estimation , 2001, The Journal of Neuroscience.

[47]  Gerit Pfuhl,et al.  Functional Split between Parietal and Entorhinal Cortices in the Rat , 2012, Neuron.

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

[49]  Eero P. Simoncelli,et al.  How MT cells analyze the motion of visual patterns , 2006, Nature Neuroscience.

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

[51]  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.

[52]  Edward T. Bullmore,et al.  Schizophrenia, neuroimaging and connectomics , 2012, NeuroImage.

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

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

[55]  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.

[56]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[59]  Adriane E Seiffert,et al.  Functional MRI studies of human visual motion perception: texture, luminance, attention and after-effects. , 2003, Cerebral cortex.

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

[61]  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.

[62]  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.

[63]  Velia Cardin,et al.  Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. , 2010, Cerebral cortex.

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

[65]  D. Somers,et al.  Functional correlates of optic flow motion processing in Parkinson’s disease , 2014, Front. Integr. Neurosci..

[66]  Gordon E. Legge,et al.  Combining Path Integration and Remembered Landmarks When Navigating without Vision , 2013, PloS one.

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

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

[69]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

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

[71]  S J Mizumori,et al.  Finding your way in the dark: the retrosplenial cortex contributes to spatial memory and navigation without visual cues. , 2001, Behavioral neuroscience.