Adaptation to heading direction dissociates the roles of human MST and V6 in the processing of optic flow.

The extraction of optic flow cues is fundamental for successful locomotion. During forward motion, the focus of expansion (FoE), in conjunction with knowledge of eye position, indicates the direction in which the individual is heading. Therefore, it is expected that cortical brain regions that are involved in the estimation of heading will be sensitive to this feature. To characterize cortical sensitivity to the location of the FoE or, more generally, the center of flow (CoF) during visually simulated self-motion, we carried out a functional MRI (fMRI) adaptation experiment in several human visual cortical areas that are thought to be sensitive to optic flow parameters, namely, V3A, V6, MT/V5, and MST. In each trial, two optic flow patterns were sequentially presented, with the CoF located in either the same or different positions. With an adaptation design, an area sensitive to heading direction should respond more strongly to a pair of stimuli with different CoFs than to stimuli with the same CoF. Our results show such release from adaptation in areas MT/V5 and MST, and to a lesser extent V3A, suggesting the involvement of these areas in the processing of heading direction. The effect could not be explained either by differences in local motion or by attention capture. It was not observed to a significant extent in area V6 or in control area V1. The different patterns of responses observed in MST and V6, areas that are both involved in the processing of egomotion in macaques and humans, suggest distinct roles in the processing of visual cues for self-motion.

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

[2]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[3]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[4]  Andrew T. Smith,et al.  Sensitivity of human visual cortical areas to the stereoscopic depth of a moving stimulus. , 2008, Journal of vision.

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

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

[7]  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.

[8]  M. Landy,et al.  Orientation-selective adaptation to first- and second-order patterns in human visual cortex. , 2006, Journal of neurophysiology.

[9]  Angelika Lingnau,et al.  Speed encoding in human visual cortex revealed by fMRI adaptation. , 2009, Journal of vision.

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

[11]  D. Heeger,et al.  Neuronal basis of contrast discrimination , 1999, Vision Research.

[12]  H. Ashida,et al.  FMRI adaptation reveals separate mechanisms for first-order and second-order motion. , 2007, Journal of neurophysiology.

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

[14]  A. Verri,et al.  First-order analysis of optical flow in monkey brain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[15]  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.

[16]  S. Zeki Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey , 1974, The Journal of physiology.

[17]  R. Tootell,et al.  Anatomical evidence for MT and additional cortical visual areas in humans. , 1995, Cerebral cortex.

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

[19]  G. Orban,et al.  Laminar analysis of motion information processing in macaque V5 , 1989, Brain Research.

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

[21]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[24]  M W Greenlee,et al.  Human cortical areas underlying the perception of optic flow: brain imaging studies. , 2000, International review of neurobiology.

[25]  J. Kaas,et al.  A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[26]  G. Orban,et al.  Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex , 2002, Science.

[27]  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.

[28]  Frank Bremmer,et al.  ã Federation of European Neuroscience Societies Heading encoding in the macaque ventral intraparietal area (VIP) , 2022 .

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

[30]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[31]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[32]  A. T. Smith,et al.  Sensitivity to optic flow in human cortical areas MT and MST , 2006, The European journal of neuroscience.

[33]  Leslie G. Ungerleider,et al.  Multiple visual areas in the caudal superior temporal sulcus of the macaque , 1986, The Journal of comparative neurology.

[34]  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.

[35]  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.

[36]  Angelika Lingnau,et al.  Selective visual responses to expansion and rotation in the human MT complex revealed by functional magnetic resonance imaging adaptation , 2008, The European journal of neuroscience.

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

[38]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

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

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

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

[42]  Takeo Watanabe,et al.  Separate Processing of Different Global-Motion Structures in Visual Cortex Is Revealed by fMRI , 2005, Current Biology.

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

[44]  Michael J. Constantino,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008 .

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

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

[47]  Frank Bremmer,et al.  Interaction of linear vestibular and visual stimulation in the macaque ventral intraparietal area (VIP) , 2002, The European journal of neuroscience.

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

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

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

[51]  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.

[52]  G. DeAngelis,et al.  Multimodal Coding of Three-Dimensional Rotation and Translation in Area MSTd: Comparison of Visual and Vestibular Selectivity , 2007, The Journal of Neuroscience.

[53]  S. Rushton,et al.  Optic Flow Processing for the Assessment of Object Movement during Ego Movement , 2009, Current Biology.

[54]  Jonas Larsson,et al.  fMRI repetition suppression: neuronal adaptation or stimulus expectation? , 2012, Cerebral cortex.

[55]  Jody C. Culham,et al.  fMRI reveals a preference for near viewing in the human parieto-occipital cortex , 2007, NeuroImage.

[56]  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.

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

[58]  Tao Zhang,et al.  Parietal Area VIP Causally Influences Heading Perception during Pursuit Eye Movements , 2011, The Journal of Neuroscience.

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

[60]  C. Galletti,et al.  Neuronal mechanisms for detection of motion in the field of view , 2003, Neuropsychologia.

[61]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

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