Role of the superior temporal region in human visual motion perception.

While moving objects are usually seen using luminance (first-order) cues, humans can perceive the motion of objects via non-luminance (second-order) cues. Contrary to previous case reports, no physiological studies have elucidated distinct differences in the cortical regions involved in first- and second-order motion processes. We investigated brain responses related to these two types of motion perception in human subjects using 3 T functional magnetic resonance imaging and strictly controlled apparent motion stimulus pairs. Comparison of brain activation to moving versus static states of each motion stimulus isolated cortical activity related to each type of motion perception. We found a selective neural response to second-order motion stimulus in the anterior part of the superior temporal sulcus (STS) contralateral to stimulus presentation and cue-invariant activation of MT/V5+. No significant activation in the STS was observed by the first-order motion, even when its visibility was reduced to levels comparable to that of second-order motion. Furthermore, the STS demonstrated significant activation for highly visible motion stimulus with both first- and second-order attributes. The STS represents the cardinal structure for perception of second-order motions, although further studies are needed to elucidate the exact neural process occurring in this area.

[1]  ANDREW T SMITH,et al.  Separate Detection of Moving Luminance and Contrast Modulations: Fact or Artifact? , 1997, Vision Research.

[2]  G. Sáry,et al.  Cerebral regions processing first‐ and higher‐order motion in an opposed‐direction discrimination task , 2003, The European journal of neuroscience.

[3]  T. Allison,et al.  Temporal Cortex Activation in Humans Viewing Eye and Mouth Movements , 1998, The Journal of Neuroscience.

[4]  T D Albright,et al.  Form-cue invariant motion processing in primate visual cortex. , 1992, Science.

[5]  G. Orban,et al.  Comparative mapping of higher visual areas in monkeys and humans , 2004, Trends in Cognitive Sciences.

[6]  K. Nakayama,et al.  Impaired visual motion perception in the contralateral hemifield following unilateral posterior cerebral lesions in humans. , 1993, Brain : a journal of neurology.

[7]  Ryusuke Kakigi,et al.  Physiological evidence of interaction of first‐ and second‐order motion processes in the human visual system: A magnetoencephalographic study , 2003, Human brain mapping.

[8]  P. Cavanagh,et al.  Motion: the long and short of it. , 1989, Spatial vision.

[9]  C. Baker.  Central neural mechanisms for detecting second-order motion , 1999, Current Opinion in Neurobiology.

[10]  T. Albright,et al.  Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1 , 1997, Visual Neuroscience.

[11]  Adriane E Seiffert,et al.  Functional MRI studies of human visual motion perception: texture, luminance, attention and after-effects. , 2003, Cerebral cortex.

[12]  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.

[13]  P. Sinha,et al.  Functional neuroanatomy of biological motion perception in humans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Derrington,et al.  Separate detectors for simple and complex grating patterns? , 1985, Vision Research.

[15]  Isabelle Mareschal,et al.  A cortical locus for the processing of contrast-defined contours , 1998, Nature Neuroscience.

[16]  G. Orban,et al.  Many areas in the human brain respond to visual motion. , 1994, Journal of neurophysiology.

[17]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[18]  G. Sperling,et al.  Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[19]  L. P. O'Keefe,et al.  Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey , 1998, Visual Neuroscience.

[20]  Lucia M Vaina,et al.  First-order and second-order motion: neurological evidence for neuroanatomically distinct systems. , 2004, Progress in brain research.

[21]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

[22]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[23]  J. Mugler,et al.  Three‐dimensional magnetization‐prepared rapid gradient‐echo imaging (3D MP RAGE) , 1990, Magnetic resonance in medicine.

[24]  O. Braddick.  A short-range process in apparent motion. , 1974, Vision research.

[25]  P. McOwan,et al.  A computational model of the analysis of some first-order and second-order motion patterns by simple and complex cells , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  Alan C. Evans,et al.  Cortical specialization for processing first- and second-order motion. , 2003, Cerebral cortex.

[27]  B. Seltzer,et al.  Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex , 1995, The Journal of comparative neurology.

[28]  N R Burns,et al.  Interaction of first- and second-order direction in motion-defined motion. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[29]  Laurence R. Harris,et al.  Interactions between first- and second-order motion revealed by optokinetic nystagmus , 1999, Experimental Brain Research.

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

[31]  N E Scott-Samuel,et al.  First-order and second-order signals combine to improve perceptual accuracy. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[32]  J. Hennig,et al.  The Processing of First- and Second-Order Motion in Human Visual Cortex Assessed by Functional Magnetic Resonance Imaging (fMRI) , 1998, The Journal of Neuroscience.

[33]  George Sperling,et al.  Attention-generated apparent motion , 1995, Nature.

[34]  Marcello G P Rosa,et al.  Physiological responses of New World monkey V1 neurons to stimuli defined by coherent motion. , 2002, Cerebral cortex.

[35]  John C. Gore,et al.  Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans , 1994 .

[36]  A. Cowey,et al.  Perception of first‐ and second‐order motion: Separable neurological mechanisms? , 1999, Human brain mapping.

[37]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[38]  Z L Lu,et al.  Three-systems theory of human visual motion perception: review and update. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[39]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[40]  G. Orban,et al.  A Higher Order Motion Region in Human Inferior Parietal Lobule Evidence from fMRI , 2003, Neuron.

[41]  Takeo Watanabe,et al.  Neuroimaging of direction-selective mechanisms for second-order motion. , 2003, Journal of neurophysiology.

[42]  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.

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