Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation.

The analysis and representation of visual cues to self-motion (egomotion) is primarily associated with cortical areas MST, VIP, and (recently) cingulate sulcus visual area (CSv). Various other areas, including visual areas V6 and V6A, and vestibular areas parietoinsular vestibular cortex (PIVC), putative area 2v (p2v), and 3aNv, are also potentially suited to processing egomotion (in some cases based on multisensory cues), but it is not known whether they are in fact involved in this process. In a functional magnetic resonance imaging (fMRI) experiment, we presented human participants with 2 types of random dot kinematograms. Both contained coherent motion but one simulated egomotion while the other did not. An area in the parieto-occipital sulcus that may correspond to V6, PIVC, and p2v were all differentially responsive to egomotion-compatible visual stimuli, suggesting that they may be involved in encoding egomotion. More generally, we show that the use of such stimuli provides a simple and reliable fMRI localizer for human PIVC and p2v, which hitherto required galvanic or caloric stimulation to be identified.

[1]  A. Antal,et al.  The posterior cingulate cortex and planum temporale/parietal operculum are activated by coherent visual motion , 2008, Visual Neuroscience.

[2]  Hilary W. Heuer,et al.  Parietal Area VIP Neuronal Responses to Heading Stimuli Are Encoded in Head-Centered Coordinates , 2004, Neuron.

[3]  R. Hetherington The Perception of the Visual World , 1952 .

[4]  S. Zeki,et al.  A visuo‐somatomotor pathway through superior parietal cortex in the macaque monkey: cortical connections of areas V6 and V6A , 1998, The European journal of neuroscience.

[5]  Rüdiger Wenzel,et al.  Human Vestibular Cortex as Identified with Caloric Stimulation in Functional Magnetic Resonance Imaging , 2002, NeuroImage.

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

[7]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[8]  U Büttner,et al.  CIRCULARVECTION: PSYCHOPHYSICS AND SINGLE‐UNIT RECORDINGS IN THE MONKEY * , 1981, Annals of the New York Academy of Sciences.

[9]  Tarek A. Yousry,et al.  fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation , 2002, Experimental Brain Research.

[10]  A. Paans,et al.  Brain Activation Related to the Representations of External Space and Body Scheme in Visuomotor Control , 2001, NeuroImage.

[11]  O. Grüsser,et al.  Responses of Single Neurons in the Parietoinsular Vestibular Cortex of Primates a , 1988, Annals of the New York Academy of Sciences.

[12]  O. Grüsser,et al.  Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey , 1994, The Journal of comparative neurology.

[13]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  G. Orban,et al.  Motion-responsive regions of the human brain , 1999, Experimental Brain Research.

[15]  U. W. Buettner,et al.  Parietal cortex (2v) neuronal activity in the alert monkey during natural vestibular and optokinetic stimulation , 1978, Brain Research.

[16]  O. Grüsser,et al.  Vestibular neurones in the parieto‐insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses. , 1990, The Journal of physiology.

[17]  T. Brandt,et al.  The Vestibular Cortex: Its Locations, Functions, and Disorders , 1999, Annals of the New York Academy of Sciences.

[18]  G. DeAngelis,et al.  A functional link between area MSTd and heading perception based on vestibular signals , 2007, Nature Neuroscience.

[19]  C. Galletti,et al.  The cortical visual area V6: brain location and visual topography , 1999, The European journal of neuroscience.

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

[21]  C. Duffy,et al.  Heading representation in MST: sensory interactions and population encoding. , 2003, Journal of neurophysiology.

[22]  T. Brandt,et al.  Dominance for vestibular cortical function in the non-dominant hemisphere. , 2003, Cerebral cortex.

[23]  Daniel J. Hannon,et al.  Direction of self-motion is perceived from optical flow , 1988, Nature.

[24]  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.

[25]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

[26]  Y. Diao,et al.  Sensitivity of LS neurons to optic flow stimuli , 1997 .

[27]  G. DeAngelis,et al.  Neural correlates of multisensory cue integration in macaque MSTd , 2008, Nature Neuroscience.

[28]  A. Berthoz,et al.  Functional MRI of galvanic vestibular stimulation. , 1998, Journal of neurophysiology.

[29]  K. Amunts,et al.  The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. , 2006, Cerebral cortex.

[30]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[31]  C. Galletti,et al.  Brain location and visual topography of cortical area V6A in the macaque monkey , 1999, The European journal of neuroscience.

[32]  A. Schleicher,et al.  Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. , 2008, Cerebral cortex.

[33]  Dora E Angelaki,et al.  Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area , 2006, The Journal of Neuroscience.

[34]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[35]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. , 1991, Journal of neurophysiology.

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

[37]  N. Logothetis,et al.  Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain. , 2008, Cerebral cortex.

[38]  C. Galletti,et al.  The cortical connections of area V6: an occipito‐parietal network processing visual information , 2001, The European journal of neuroscience.

[39]  Christian Büchel,et al.  Spatial updating: how the brain keeps track of changing object locations during observer motion , 2008, Nature Neuroscience.

[40]  O. Grüsser,et al.  Is there a vestibular cortex? , 1998, Trends in Neurosciences.

[41]  Richard S. J. Frackowiak,et al.  Identification of the central vestibular projections in man: a positron emission tomography activation study , 2004, Experimental Brain Research.

[42]  G. Leichnetz Connections of the medial posterior parietal cortex (area 7m) in the monkey , 2001, The Anatomical record.

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

[44]  M. Wiesmann,et al.  Cerebral functional magnetic resonance imaging of vestibular, auditory, and nociceptive areas during galvanic stimulation , 1998, Annals of neurology.

[45]  F. Lacquaniti,et al.  Representation of Visual Gravitational Motion in the Human Vestibular Cortex , 2005, Science.

[46]  R Turner,et al.  Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T , 2004, NeuroImage.

[47]  Richard S. Frackowiak,et al.  Neural Correlates of Visual-Motion Perception as Object- or Self-motion , 2002, NeuroImage.

[48]  T. Brandt,et al.  Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. , 1998, Brain : a journal of neurology.

[49]  E. Maguire,et al.  A Temporoparietal and Prefrontal Network for Retrieving the Spatial Context of Lifelike Events , 2001, NeuroImage.

[50]  C. Baumgartner,et al.  Vestibular processing in human paramedian precuneus as shown by electrical cortical stimulation , 2004, Neurology.

[51]  P Fattori,et al.  Parietal neurons encoding visual space in a head-frame of reference. , 1992, Bollettino della Societa italiana di biologia sperimentale.

[52]  J. Gibson The perception of the visual world , 1951 .

[53]  Rüdiger Wenzel,et al.  Proprioceptive head posture-related processing in human polysensory cortical areas , 2008, NeuroImage.

[54]  D. Burr,et al.  A cortical area that responds specifically to optic flow, revealed by fMRI , 2000, Nature Neuroscience.

[55]  Mark W Greenlee,et al.  Neural correlates of visually induced self-motion illusion in depth. , 2008, Cerebral cortex.

[56]  Guldin Wo,et al.  Is there a vestibular cortex , 1998 .

[57]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[58]  C. Galletti,et al.  Functional Demarcation of a Border Between Areas V6 and V6A in the Superior Parietal Gyrus of the Macaque Monkey , 1996, The European journal of neuroscience.

[59]  Simo Vanni,et al.  Central luminance flicker can activate peripheral retinotopic representation , 2007, NeuroImage.

[60]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[61]  J Duysens,et al.  Neurons in the ventral intraparietal area of awake macaque monkey closely resemble neurons in the dorsal part of the medial superior temporal area in their responses to optic flow patterns. , 1996, Journal of neurophysiology.

[62]  Hiroshi Yamazaki,et al.  Cortical activation during optokinetic stimulation – an fMRI study , 2009, Acta oto-laryngologica.

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

[64]  K. Amunts,et al.  Identifying human parieto‐insular vestibular cortex using fMRI and cytoarchitectonic mapping , 2006, Human brain mapping.

[65]  C. Galletti,et al.  Functional Properties of Neurons in the Anterior Bank of the Parieto‐occipital Sulcus of the Macaque Monkey , 1991, The European journal of neuroscience.

[66]  T. Brandt,et al.  Sensory system interactions during simultaneous vestibular and visual stimulation in PET , 2002, Human brain mapping.

[67]  K. Tanaka,et al.  Directionally selective response of cells in the middle temporal area (MT) of the macaque monkey to the movement of equiluminous opponent color stimuli , 2004, Experimental Brain Research.

[68]  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.