The integration of higher order form and motion by the human brain

Our experience with a dynamic environment has tuned our visual system to use form and motion as complementary sources of information for object recognition. To identify the neural systems involved in integrating form and motion information during dynamic object processing, we used an fMRI adaptation paradigm which factorially manipulated form and motion repetition. Observers were sequentially presented with pairs of rotating novel objects in which the form or rotation direction in depth could be repeated. They were required to discriminate either dimension of the second target object, while the first object served as a form and/or motion prime. At the behavioural level, observers were faster to recognize the target or discriminate its direction when primed by the same form. Importantly, this form priming effect was enhanced when prime and target objects rotated in the same direction. At the neural level, the two priming effects (i.e., the main effect of form repetition and the interaction between form and motion repetition) were associated with reduced activations in distinct brain regions. Bilateral lateral occipital regions exhibited reduced activation when form was repeated irrespective of rotation direction. In contrast, bilateral anterior fusiform and posterior middle temporal regions (overlapping with hMT+/V5) regions showed an adaptation effect that depended on both form and motion direction. Thus, the current results reveal a visual processing hierarchy with lateral occipito-temporal cortex representing an object's 3D structure, and anterior fusiform and posterior middle temporal regions being involved in spatio-temporal integration of form and motion during dynamic object processing.

[1]  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.

[2]  G. Orban,et al.  The kinetic occipital (KO) region in man: an fMRI study. , 1997, Cerebral cortex.

[3]  W. Singer,et al.  The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery , 1998, The European journal of neuroscience.

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

[5]  G. Pike,et al.  Recognizing moving faces: The relative contribution of motion and perspective view information. , 1997 .

[6]  E. DeYoe,et al.  Segregation of efferent connections and receptive field properties in visual area V2 of the macaque , 1985, Nature.

[7]  Stefan Treue,et al.  Human perception of structure from motion , 1991, Vision Research.

[8]  S. Ullman,et al.  The interpretation of visual motion , 1977 .

[9]  Nikos K. Logothetis,et al.  Motion Processing in the Macaque: Revisited with Functional Magnetic Resonance Imaging , 2001, The Journal of Neuroscience.

[10]  D. Marr,et al.  Representation and recognition of the movements of shapes , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[11]  Hideo Sakata,et al.  Functional properties of rotation-sensitive neurons in the posterior parietal association cortex of the monkey , 1994, Experimental Brain Research.

[12]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  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.

[14]  Paul Schrater,et al.  Shape perception reduces activity in human primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. Weller Two cortical visual systems in Old World and New World primates. , 1988, Progress in brain research.

[16]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[17]  Guy A. Orban,et al.  Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI , 2003, Neuropsychologia.

[18]  T. Hendler,et al.  Visuo-haptic object-related activation in the ventral visual pathway , 2001, Nature Neuroscience.

[19]  Nicholas J. Priebe,et al.  Constraints on the source of short-term motion adaptation in macaque area MT. I. the role of input and intrinsic mechanisms. , 2002, Journal of neurophysiology.

[20]  A Berthoz,et al.  Visual perception of motion and 3-D structure from motion: an fMRI study. , 2000, Cerebral cortex.

[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]  Kazuhiko Yokosawa,et al.  Efficient Extrapolation of the View with a Dynamic and Predictive Stimulus , 2003, Perception.

[23]  R. Andersen,et al.  Response of MSTd neurons to simulated 3D orientation of rotating planes. , 2002, Journal of neurophysiology.

[24]  K. H. Britten,et al.  Motion adaptation in area MT. , 2002, Journal of neurophysiology.

[25]  H. Bülthoff,et al.  Effects of temporal association on recognition memory , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[26]  H. Bülthoff,et al.  Learning to recognize objects , 1999, Trends in Cognitive Sciences.

[27]  E. Macaluso,et al.  Neural basis for priming of pop-out during visual search revealed with fMRI. , 2007, Cerebral cortex.

[28]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[29]  H. Bülthoff,et al.  Representation of the perceived 3-D object shape in the human lateral occipital complex. , 2003, Cerebral cortex.

[30]  D. Norris,et al.  THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 1996, 49A (1), 80 ± 115 Unchained Memory: Error Patterns Rule out Chaining Models of Immediate Serial Recall , 2022 .

[31]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[32]  Scott O. Murray,et al.  Processing Shape, Motion and Three-dimensional Shape-from-motion in the Human Cortex , 2003 .

[33]  H. Sakata,et al.  Parietal cortical neurons responding to rotary movement of visual stimulus in space , 2004, Experimental Brain Research.

[34]  David J. Heeger,et al.  Pattern-motion responses in human visual cortex , 2002, Nature Neuroscience.

[35]  M. H. Kelly,et al.  Explorations of representational momentum , 1987, Cognitive Psychology.

[36]  G. A. Calvert,et al.  Hemodynamic studies of audio-visual interactions , 2003 .

[37]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[38]  Pia Rotshtein,et al.  On-line attentional selection from competing stimuli in opposite visual fields: effects on human visual cortex and control processes. , 2006, Journal of neurophysiology.

[39]  James V. Stone Object recognition using spatiotemporal signatures , 1998, Vision Research.

[40]  S. Zeki Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. , 1978, The Journal of physiology.

[41]  Alan C. Evans,et al.  An MRI-based stereotactic atlas from 250 young normal subjects , 1992 .

[42]  Nicholas J. Priebe,et al.  Constraints on the source of short-term motion adaptation in macaque area MT. II. tuning of neural circuit mechanisms. , 2002, Journal of neurophysiology.

[43]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[44]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[45]  Bettina Sorger,et al.  Human Cortical Object Recognition from a Visual Motion Flowfield , 2003, The Journal of Neuroscience.

[46]  E. Reed The Ecological Approach to Visual Perception , 1989 .

[47]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[48]  T. Hendler,et al.  Contrast sensitivity in human visual areas and its relationship to object recognition. , 2002, Journal of neurophysiology.

[49]  Michael Erb,et al.  Object-selective responses in the human motion area MT/MST , 2002, Nature Neuroscience.

[50]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[51]  D. Heeger,et al.  Neuronal Basis of the Motion Aftereffect Reconsidered , 2001, Neuron.

[52]  Frans A. J. Verstraten,et al.  Perceptual manifestations of fast neural plasticity: Motion priming, rapid motion aftereffect and perceptual sensitization , 2005, Vision Research.

[53]  Taosheng Liu,et al.  Explicit and implicit memory for rotating objects. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[54]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

[56]  Michael J Tarr,et al.  Structural Similarity and Spatiotemporal Noise Effects on Learning Dynamic Novel Objects , 2006, Perception.

[57]  James V. Stone,et al.  Object recognition: view-specificity and motion-specificity , 1999, Vision Research.

[58]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[59]  Nikos K. Logothetis,et al.  Three-Dimensional Shape Representation in Monkey Cortex , 2002, Neuron.

[60]  M. Tarr,et al.  Rotation direction affects object recognition , 2004, Vision Research.

[61]  Matthew W Self,et al.  The integration of colour and motion by the human visual brain. , 2005, Cerebral cortex.