Direct and indirect parieto-medial temporal pathways for spatial navigation in humans: evidence from resting-state functional connectivity

Anatomical and functional findings in primates suggest the existence of a dedicated parieto-medial temporal pathway for spatial navigation, consisting of both direct and indirect projections from the caudal inferior parietal lobe (cIPL) to the hippocampus and the parahippocampal cortex, with indirect projections relaying through the posterior cingulate and retrosplenial cortex. This neural network is largely unexplored in humans. This study aimed at testing the existence of a parieto-medial temporal pathway for spatial navigation in humans. We explored the cortical connectivity patterns of the parahippocampal place area (PPA), the retrosplenial cortex (RSC), and the hippocampus (HC) using resting-state functional connectivity MRI. Our results demonstrate the existence of connections between the medial temporal lobe structures, i.e., PPA and HC, and the angular gyrus (AG), the human homologue of cIPL, as well as between RSC and AG. These connectivity patterns seem to reflect the direct and the indirect projections found in primates from cIPL to the medial temporal lobe. Such a result deserves feasible considerations to better understand the brain networks underpinning human spatial navigation.

[1]  Emily S. Cross,et al.  Disentangling neural processes of egocentric and allocentric mental spatial transformations using whole-body photos of self and other , 2015, NeuroImage.

[2]  Mortimer Mishkin,et al.  Mapping the primate visual system with [2-14C]deoxyglucose. , 1982, Science.

[3]  G. Committeri,et al.  Distributed cognitive maps reflecting real distances between places and views in the human brain , 2014, Front. Hum. Neurosci..

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

[5]  M. Behrmann,et al.  Updating of locations during whole-body rotations in patients with hemispatial neglect , 2001, Cognitive, affective & behavioral neuroscience.

[6]  V. Mildner The cognitive neuroscience of human communication , 2007 .

[7]  A. Wunderlich,et al.  Brain activation during human navigation: gender-different neural networks as substrate of performance , 2000, Nature Neuroscience.

[8]  Martin I. Sereno,et al.  The Human Homologue of Macaque Area V6A , 2012 .

[9]  Jonas Persson,et al.  Behavioural Brain Research , 2013 .

[10]  M. Sereno,et al.  A human parietal face area contains aligned head-centered visual and tactile maps , 2006, Nature Neuroscience.

[11]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[12]  Diego Kaski,et al.  Temporoparietal encoding of space and time during vestibular-guided orientation , 2015, Brain : a journal of neurology.

[13]  G. Iaria,et al.  Representational neglect and navigation in real space , 2005, Neuropsychologia.

[14]  Alain Berthoz,et al.  Selective role of lingual/parahippocampal gyrus and retrosplenial complex in spatial memory across viewpoint changes relative to the environmental reference frame , 2013, Behavioural Brain Research.

[15]  Eleanor A. Maguire,et al.  Scenes , Spaces , and Memory Traces : What Does the Hippocampus Do ? , 2015 .

[16]  Laura Piccardi,et al.  Sex differences in a landmark environmental re-orientation task only during the learning phase , 2011, Neuroscience Letters.

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

[18]  Isabelle D. Cherney,et al.  Mapping Out Spatial Ability: Sex Differences in Way-Finding Navigation , 2008, Perceptual and motor skills.

[19]  C. Guariglia,et al.  Environmental orientation and navigation in different types of unilateral neglect , 2010, Experimental Brain Research.

[20]  Fenna M. Krienen,et al.  Opportunities and limitations of intrinsic functional connectivity MRI , 2013, Nature Neuroscience.

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

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

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

[24]  Gaspare Galati,et al.  Functional connectivity between posterior hippocampus and retrosplenial complex predicts individual differences in navigational ability , 2016, Hippocampus.

[25]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: III. Cortical efferents , 2003, The Journal of comparative neurology.

[26]  D. Nico,et al.  Landmark based navigation in brain-damaged patients with neglect , 2008, Neuropsychologia.

[27]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[28]  Federico Nemmi,et al.  A penny for your thoughts! patterns of fMRI activity reveal the content and the spatial topography of visual mental images , 2015, Human brain mapping.

[29]  Svetlana S. Georgieva,et al.  The Processing of Three-Dimensional Shape from Disparity in the Human Brain , 2009, The Journal of Neuroscience.

[30]  Andrew T. Smith,et al.  The Representation of Egomotion in the Human Brain , 2008, Current Biology.

[31]  J. Doudna,et al.  Structural and mechanistic insights into hepatitis C viral translation initiation , 2007, Nature Reviews Microbiology.

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

[33]  M. Goodale,et al.  The visual brain in action , 1995 .

[34]  K. Rockland,et al.  Inferior parietal lobule projections to the presubiculum and neighboring ventromedial temporal cortical areas , 2000, The Journal of comparative neurology.

[35]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

[36]  Gaspare Galati,et al.  Resting-state connectivity and functional specialization in human medial parieto-occipital cortex , 2014, Brain Structure and Function.

[37]  Arthur W. Toga,et al.  A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development The International Consortium for Brain Mapping (ICBM) , 1995, NeuroImage.

[38]  A. Bartels,et al.  Parietal Cortex Codes for Egocentric Space beyond the Field of View , 2012, Current Biology.

[39]  H. Eichenbaum,et al.  Towards a functional organization of episodic memory in the medial temporal lobe , 2012, Neuroscience & Biobehavioral Reviews.

[40]  Federico Nemmi,et al.  Segregation of neural circuits involved in spatial learning in reaching and navigational space , 2013, Neuropsychologia.

[41]  A. Sirigu,et al.  Pure Topographical Disorientation: A Definition and Anatomical Basis , 1987, Cortex.

[42]  Paola Verde,et al.  Gender differences in navigational memory: pilots vs. nonpilots. , 2015, Aerospace medicine and human performance.

[43]  John O'Keefe,et al.  The cognitive map as a hippocampus , 1979, Behavioral and Brain Sciences.

[44]  Alain Berthoz,et al.  Role of the human retrosplenial cortex/parieto-occipital sulcus in perspective priming , 2016, NeuroImage.

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

[46]  H. Eichenbaum,et al.  Complementary Roles of Hippocampus and Medial Entorhinal Cortex in Episodic Memory , 2008, Neural plasticity.

[47]  L. Squire,et al.  Memory, scene construction, and the human hippocampus , 2015, Proceedings of the National Academy of Sciences.

[48]  D. Pandya,et al.  Fiber system linking the mid‐dorsolateral frontal cortex with the retrosplenial/presubicular region in the rhesus monkey , 1999, The Journal of comparative neurology.

[49]  Gaspare Galati,et al.  Where did you “left” Piazza del Popolo? At your “right” temporo-parietal junction , 2015, Cortex.

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

[51]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

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

[53]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[54]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[55]  E. C. Ritchie,et al.  Gender Differences , 1981, Language in Society.

[56]  Brenda Milner,et al.  The medial temporal-lobe amnesic syndrome. , 2005, The Psychiatric clinics of North America.

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

[58]  M. Stark,et al.  Impairment of an Egocentric Map of Locations: Implications for Perception and Action , 1996 .

[59]  L. Squire,et al.  The cognitive neuroscience of human memory since H.M. , 2011, Annual review of neuroscience.

[60]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[61]  Christian F. Doeller,et al.  Imagining being somewhere else: neural basis of changing perspective in space. , 2012, Cerebral cortex.

[62]  M. Corbetta,et al.  Decision and action planning signals in human posterior parietal cortex during delayed perceptual choices , 2014, The European journal of neuroscience.

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

[64]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[65]  Maddalena Boccia,et al.  Navigating toward a novel environment from a route or survey perspective: neural correlates and context-dependent connectivity , 2015, Brain Structure and Function.

[66]  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.

[67]  A. Berthoz,et al.  Mental navigation along memorized routes activates the hippocampus, precuneus, and insula , 1997, Neuroreport.

[68]  M. Petrides,et al.  Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps , 2007, The European journal of neuroscience.

[69]  H. Eichenbaum,et al.  From Conditioning to Conscious Recollection , 2001 .

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

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

[72]  N. Cohen From Conditioning to Conscious Recollection Memory Systems of the Brain. Oxford Psychology Series, Volume 35. , 2001 .

[73]  Jeffrey S. Taube,et al.  Impaired Head Direction Cell Representation in the Anterodorsal Thalamus after Lesions of the Retrosplenial Cortex , 2010, The Journal of Neuroscience.

[74]  K. Rockland,et al.  Some temporal and parietal cortical connections converge in CA1 of the primate hippocampus. , 1999, Cerebral cortex.

[75]  C. Guariglia,et al.  Neuropsychology of Environmental Navigation in Humans: Review and Meta-Analysis of fMRI Studies in Healthy Participants , 2014, Neuropsychology Review.

[76]  Qiyong Guo,et al.  Retinotopic mapping of the peripheral visual field to human visual cortex by functional magnetic resonance imaging , 2012, Human brain mapping.

[77]  Aldo Genovesio,et al.  Integration of retinal disparity and fixation-distance related signals toward an egocentric coding of distance in the posterior parietal cortex of primates. , 2004, Journal of neurophysiology.