Neural correlates of egocentric and allocentric frames of reference combined with metric and non-metric spatial relations

Spatial relations (SRs: coordinate/metric vs categorical/non metric) and frames of reference (FoRs: egocentric/body vs allocentric/external element) represent the building blocks underlying any spatial representation. In the present 7-T fMRI study we have identified for the first time the neural correlates of the spatial representations emerging from the combination of the two dimensions. The direct comparison between the different spatial representations revealed a bilateral fronto-parietal network, mainly right sided, that was more involved in the egocentric categorical representations. A right fronto-parietal circuitry was specialized for egocentric coordinate representations. A bilateral occipital network was more involved in the allocentric categorical representations. Finally, a smaller part of this bilateral network (i.e. Calcarine Sulcus and Lingual Gyrus), along with the right Supramarginal and Inferior Frontal gyri, supported the allocentric coordinate representations. The fact that some areas were more involved in a spatial representation than in others reveals how our brain builds adaptive spatial representations in order to effectively react to specific environmental needs and task demands.

[1]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[2]  Jérôme Prado,et al.  Heightened activity in a key region of the ventral attention network is linked to reduced activity in a key region of the dorsal attention network during unexpected shifts of covert visual spatial attention , 2012, NeuroImage.

[3]  A. Postma,et al.  Frames of reference and categorical/coordinate spatial relations in a “what was where” task , 2016, Experimental Brain Research.

[4]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Hattingen,et al.  The U Sign: Tenth Landmark to the Central Region on Brain Surface Reformatted MR Imaging , 2013, American Journal of Neuroradiology.

[6]  Matthew F. S. Rushworth,et al.  Attention systems and the organization of the human parietal cortex , 2001, NeuroImage.

[7]  S. Kosslyn You can play 20 questions with nature and win: Categorical versus coordinate spatial relations as a case study , 2006, Neuropsychologia.

[8]  A. Berthoz,et al.  Reference Frames for Spatial Cognition: Different Brain Areas are Involved in Viewer-, Object-, and Landmark-Centered Judgments About Object Location , 2004, Journal of Cognitive Neuroscience.

[9]  G. Vallar,et al.  Parietal versus temporal lobe components in spatial cognition: Setting the mid-point of a horizontal line. , 2009, Journal of neuropsychology.

[10]  M. Perenin,et al.  Optic Ataxia and Unilateral Neglect: Clinical Evidence for Dissociable Spatial Functions in Posterior Parietal Cortex , 1997 .

[11]  A. Sack Parietal cortex and spatial cognition , 2009, Behavioural Brain Research.

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

[13]  J. Paillard Motor and representational framing of space , 1991 .

[14]  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.

[15]  Alain Berthoz,et al.  A fronto-parietal system for computing the egocentric spatial frame of reference in humans , 1999, Experimental Brain Research.

[16]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[17]  Nick F. Ramsey,et al.  Interactions between ego- and allocentric neuronal representations of space , 2006, NeuroImage.

[18]  Roberta L. Klatzky,et al.  Allocentric and Egocentric Spatial Representations: Definitions, Distinctions, and Interconnections , 1998, Spatial Cognition.

[19]  Stephan Eliez,et al.  A volumetric study of parietal lobe subregions in Turner syndrome. , 2004, Developmental medicine and child neurology.

[20]  R. Thompson A Note on Restricted Maximum Likelihood Estimation with an Alternative Outlier Model , 1985 .

[21]  S. Bricogne,et al.  Neural Correlates of Topographic Mental Exploration: The Impact of Route versus Survey Perspective Learning , 2000, NeuroImage.

[22]  Lauren Davidson,et al.  A Sense of Space , 2016 .

[23]  S. Dehaene,et al.  Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe , 2002, Neuron.

[24]  Leslie G. Ungerleider,et al.  Dominance of the right hemisphere and role of area 2 in human kinesthesia. , 2005, Journal of neurophysiology.

[25]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[26]  M. D’Esposito,et al.  An Area within Human Ventral Cortex Sensitive to “Building” Stimuli Evidence and Implications , 1998, Neuron.

[27]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[28]  Stephen M. Rao,et al.  Neural Basis of Endogenous and Exogenous Spatial Orienting: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[29]  Albert Postma,et al.  Categorical and coordinate spatial relations in working memory: An fMRI study , 2009, Brain Research.

[30]  Juan Lupiáñez,et al.  Two cognitive and neural systems for endogenous and exogenous spatial attention , 2013, Behavioural Brain Research.

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

[32]  S. Zeki,et al.  The neurology of saccades and covert shifts in spatial attention: an event-related fMRI study. , 2000, Brain : a journal of neurology.

[33]  N. Burgess,et al.  Spatial memory: how egocentric and allocentric combine , 2006, Trends in Cognitive Sciences.

[34]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[35]  G. Rizzolatti,et al.  Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses , 1981, Behavioural Brain Research.

[36]  Leeanne M. Carey,et al.  The Right Supramarginal Gyrus Is Important for Proprioception in Healthy and Stroke-Affected Participants: A Functional MRI Study , 2015, Front. Neurol..

[37]  S. Kosslyn Seeing and imagining in the cerebral hemispheres: a computational approach. , 1987, Psychological review.

[38]  Gereon R. Fink,et al.  Human medial intraparietal cortex subserves visuomotor coordinate transformation , 2004, NeuroImage.

[39]  Scott T. Grafton,et al.  Cortical topography of human anterior intraparietal cortex active during visually guided grasping. , 2005, Brain research. Cognitive brain research.

[40]  Bruce Bridgeman,et al.  Processing spatial information in the sensorimotor branch of the visual system , 2000, Vision Research.

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

[42]  M. Yașargil,et al.  Topographic anatomy of the insular region. , 1999, Journal of neurosurgery.

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

[44]  Fred W. Mast,et al.  The neural basis of the egocentric and allocentric spatial frame of reference , 2007, Brain Research.

[45]  Jean Decety,et al.  Leader or follower? Involvement of the inferior parietal lobule in agency , 2002, Neuroreport.

[46]  Jon Driver,et al.  Object-Centered Visual Neglect, or Relative Egocentric Neglect? , 2000, Journal of Cognitive Neuroscience.

[47]  Volker H. Franz,et al.  When is grasping affected by the Müller-Lyer illusion? A quantitative review , 2009, Neuropsychologia.

[48]  J. Sanes,et al.  Spatial coding of visual and somatic sensory information in body‐centred coordinates , 2001, The European journal of neuroscience.

[49]  Thomas J. Ross,et al.  Neuroanatomical dissociation between bottom–up and top–down processes of visuospatial selective attention , 2006, NeuroImage.

[50]  O. Blanke,et al.  Location of the human frontal eye field as defined by electrical cortical stimulation: anatomical, functional and electrophysiological characteristics , 2000, Neuroreport.

[51]  Maurizio Gentilucci,et al.  Visually guided pointing, the Müller-Lyer illusion, and the functional interpretation of the dorsal-ventral split: Conclusions from 33 independent studies , 2008, Neuroscience & Biobehavioral Reviews.

[52]  M. Goodale,et al.  Neural Substrates of Visual Spatial Coding and Visual Feedback Control for Hand Movements in Allocentric and Target-Directed Tasks , 2011, Front. Hum. Neurosci..

[53]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[54]  Alexandre Pouget,et al.  Basis Functions for Object-Centered Representations , 2003, Neuron.

[55]  Li Fei-Fei,et al.  Simple line drawings suffice for functional MRI decoding of natural scene categories , 2011, Proceedings of the National Academy of Sciences.

[56]  Anjan Chatterjee,et al.  The Neural Basis for Spatial Relations , 2010, Journal of Cognitive Neuroscience.

[57]  J Hyvärinen,et al.  Regional distribution of functions in parietal association area 7 of the monkey. , 1981, Brain research.

[58]  C Dohle,et al.  Human anterior intraparietal area subserves prehension , 1998, Neurology.

[59]  O J Grüsser,et al.  Localization and responses of neurones in the parieto‐insular vestibular cortex of awake monkeys (Macaca fascicularis). , 1990, The Journal of physiology.

[60]  Steen Moeller,et al.  T 1 weighted brain images at 7 Tesla unbiased for Proton Density, T 2 ⁎ contrast and RF coil receive B 1 sensitivity with simultaneous vessel visualization , 2009, NeuroImage.

[61]  Leslie G. Ungerleider,et al.  The Effect of Face Inversion on Activity in Human Neural Systems for Face and Object Perception , 1999, Neuron.

[62]  S. Swinnen,et al.  The neural basis of central proprioceptive processing in older versus younger adults: An important sensory role for right putamen , 2012, Human brain mapping.

[63]  J. Mohr,et al.  Inaccurate reaching associated with a superior parietal lobe tumor , 1978, Neurology.

[64]  S. Levinson,et al.  Can language restructure cognition? The case for space , 2004, Trends in Cognitive Sciences.

[65]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[66]  Fei-Fei Li,et al.  Differential connectivity within the Parahippocampal Place Area , 2013, NeuroImage.

[67]  Brian Everitt,et al.  A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus , 2006, Human brain mapping.

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

[69]  Daniel D. Dilks,et al.  The occipital place area represents the local elements of scenes , 2016, NeuroImage.

[70]  Albert Postma,et al.  Quantifying the interactions between allo- and egocentric representations of space. , 2005, Acta psychologica.

[71]  A. Postma,et al.  On the hemispheric specialization for categorical and coordinate spatial relations: a review of the current evidence , 2003, Neuropsychologia.

[72]  Jean-Francois Mangin,et al.  Automatized clustering and functional geometry of human parietofrontal networks for language, space, and number , 2004, NeuroImage.

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

[74]  Alan Cowey,et al.  On the usefulness of ‘what’ and ‘where’ pathways in vision , 2011, Trends in Cognitive Sciences.

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

[76]  A. Berthoz,et al.  The neural basis of egocentric and allocentric coding of space in humans: a functional magnetic resonance study , 2000, Experimental Brain Research.

[77]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[78]  Albert Postma,et al.  How coordinate and categorical spatial relations combine with egocentric and allocentric reference frames in a motor task: Effects of delay and stimuli characteristics , 2015, Behavioural Brain Research.

[79]  A. Postma,et al.  eview ateralized perception : The role of attention in spatial elation processing , 2014 .

[80]  M. Corbetta,et al.  Areas Involved in Encoding and Applying Directional Expectations to Moving Objects , 1999, The Journal of Neuroscience.

[81]  T. Paus,et al.  Cortical regions involved in eye movements, shifts of attention, and gaze perception , 2005, Human brain mapping.

[82]  Tina Iachini,et al.  The lost ability to find the way: topographical disorientation after a left brain lesion. , 2014, Neuropsychology.

[83]  C. Gross,et al.  A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields , 1993, Experimental Brain Research.

[84]  Ineke J M van der Ham,et al.  The relationship between allocentric and egocentric frames of reference and categorical and coordinate spatial information processing , 2011, Quarterly journal of experimental psychology.

[85]  Juhani Hyva¨rinen Regional distribution of functions in parietal association area 7 of the monkey , 1981, Brain Research.

[86]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[87]  C. Segebarth,et al.  Categorical and coordinate spatial relations: fMRI evidence for hemispheric specialization. , 1999, Neuroreport.

[88]  J. Douglas Crawford,et al.  Allocentric versus Egocentric Representation of Remembered Reach Targets in Human Cortex , 2014, The Journal of Neuroscience.

[89]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[90]  Natalia Y. Bilenko,et al.  The “Parahippocampal Place Area” Responds Preferentially to High Spatial Frequencies in Humans and Monkeys , 2011, PLoS biology.

[91]  B. Bridgeman,et al.  Interaction of cognitive and sensorimotor maps of visual space , 1997, Perception & psychophysics.

[92]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[93]  Volkmar Glauche,et al.  Functional properties and interaction of the anterior and posterior intraparietal areas in humans , 2003, The European journal of neuroscience.

[94]  S. Slotnick,et al.  Prefrontal cortex hemispheric specialization for categorical and coordinate visual spatial memory , 2006, Neuropsychologia.

[95]  Leslie G. Ungerleider,et al.  Posterior parietal cortex and the filtering of distractors , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[96]  Luigi Trojano,et al.  Lateralization of egocentric and allocentric spatial processing after parietal brain lesions , 2009, Brain and Cognition.

[97]  M. Perenin,et al.  Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. , 1988, Brain : a journal of neurology.

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

[99]  M. Petrides Neuroanatomy of Language Regions of the Human Brain , 2013 .

[100]  Qi Chen,et al.  Common and specific neural correlates underlying the spatial congruency effect induced by the egocentric and allocentric reference frame , 2017, Human brain mapping.

[101]  Albert Postma,et al.  Frames of reference and categorical and coordinate spatial relations: a hierarchical organisation , 2011, Experimental Brain Research.

[102]  William C. Ogden,et al.  Attended and unattended processing modes: The role of set for spatial location , 2014 .