Visual detection of motion speed in humans: spatiotemporal analysis by fMRI and MEG

Humans take a long time to respond to the slow visual motion of an object. It is not known what neural mechanism causes this delay. We measured magnetoencephalographic neural responses to light spot motion onset within a wide speed range (0.4–500°/sec) and compared these with human reaction times (RTs). The mean response latency was inversely related to the speed of motion up to 100°/sec, whereas the amplitude increased with the speed. The response property at the speed of 500°/sec was different from that at the other speeds. The speed‐related latency change was observed when the motion duration was 10 msec or longer in the speed range between 5 and 500°/sec, indicating that the response is directly related to the speed itself. The source of the response was estimated to be around the human MT+ and was validated by functional magnetic imaging study using the same stimuli. The results indicate that the speed of motion is encoded in the neural activity of MT+ and that it can be detected within 10 msec of motion observation. RT to the same motion onset was also inversely related to the speed of motion but the delay could not be explained by the magnetic response latency change. Instead, the reciprocal of RT was linearly related to the reciprocal of the magnetic response latency, suggesting that the visual process interacts with other neural processes for decision and motor preparation. Hum. Brain Mapping 16:104–118, 2002. © 2002 Wiley‐Liss, Inc.

[1]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[2]  S. Mateeff,et al.  Temporal thresholds and reaction time to changes in velocity of visual motion , 1995, Vision Research.

[3]  R J Ilmoniemi,et al.  Spatiotemporal activity of a cortical network for processing visual motion revealed by MEG and fMRI. , 1999, Journal of neurophysiology.

[4]  R. S. J. Frackowiak,et al.  The Activity in Human Areas V1/V2, V3, and V5 during the Perception of Coherent and Incoherent Motion , 1996, NeuroImage.

[5]  R. Glantz,et al.  Directional selectivity in a nonspiking interneuron of the crayfish optic lobe: evaluation of a linear model. , 1994, Journal of neurophysiology.

[6]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

[7]  A. V. van den Berg,et al.  Reaction times to motion onset and motion detection thresholds reflect the properties of bilocal motion detectors. , 1989, Vision research.

[8]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[9]  D. Heeger,et al.  Task-related modulation of visual cortex. , 2000, Journal of neurophysiology.

[10]  J. Sarvas.  Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

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

[12]  Maninder K. Kahlon,et al.  Visual Motion Analysis for Pursuit Eye Movements in Area MT of Macaque Monkeys , 1999, The Journal of Neuroscience.

[13]  V. Jousmäki,et al.  Activation trace lifetime of human cortical responses evoked by apparent visual motion , 1997, Neuroscience Letters.

[14]  R Kakigi,et al.  Human visual motion areas determined individually by magnetoencephalography and 3D magnetic resonance imaging , 2000, Human brain mapping.

[15]  S. Yamane,et al.  Neural activity in cortical area MST of alert monkey during ocular following responses. , 1994, Journal of neurophysiology.

[16]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[17]  R. Kakigi,et al.  Magnetic response of human extrastriate cortex in the detection of coherent and incoherent motion , 2000, Neuroscience.

[18]  J. Gold,et al.  Representation of a perceptual decision in developing oculomotor commands , 2000, Nature.

[19]  G. Orban,et al.  Human velocity and direction discrimination measured with random dot patterns , 1988, Vision Research.

[20]  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.

[21]  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.

[22]  Christo Pantev,et al.  Reproducibility and Validity of Neuromagnetic Source Localization Using A Large Array Biomagnetometer , 1991 .

[23]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

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

[25]  K Cheng,et al.  Human cortical regions activated by wide-field visual motion: an H2(15)O PET study. , 1995, Journal of neurophysiology.

[26]  S. Ogawa,et al.  Magnetic resonance imaging of blood vessels at high fields: In vivo and in vitro measurements and image simulation , 1990, Magnetic resonance in medicine.

[27]  Charles S. Myers,et al.  On reaction times. , 1909 .

[28]  H Suzuki,et al.  Human cortical area responding to stimuli in apparent motion , 1997, Neuroreport.

[29]  S. Mateeff,et al.  The relation between the velocity of visual motion and the reaction time to motion onset and offset , 1992, Vision Research.

[30]  C. N. Guy,et al.  The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex. , 1995, Brain : a journal of neurology.

[31]  O. Braddick,et al.  What is Noise for the Motion System? , 1996, Vision Research.

[32]  R. Sekuler,et al.  Detection of changes in speed and direction of motion: Reaction time analysis , 1993, Perception & psychophysics.

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

[34]  M. Korth,et al.  The sequential processing of visual motion in the human electroretinogram and visual evoked potential , 2000, Visual Neuroscience.

[35]  Alexander Thiele,et al.  Speed skills: measuring the visual speed analyzing properties of primate MT neurons , 2001, Nature Neuroscience.

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

[37]  R Sekuler,et al.  Models of stimulus uncertainty in motion perception. , 1980, Psychological review.

[38]  G. Orban,et al.  Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. , 1999, Journal of neurophysiology.

[39]  Magnetoencephalography—Update and Future Hopes , 1983 .

[40]  M. Fahle,et al.  Why do isoluminant stimuli appear slower? , 1988, Journal of the Optical Society of America. A, Optics and image science.

[41]  David C. Burr,et al.  Reaction time to motion onset of luminance and chromatic gratings is determined by perceived speed , 1998, Vision Research.

[42]  E Donchin,et al.  A metric for thought: a comparison of P300 latency and reaction time. , 1981, Science.

[43]  T Elbert,et al.  The cortical representation of object motion in man is inter‐individually variable , 1996, Neuroreport.

[44]  Y. Ejima,et al.  Analysis of simple reaction time to sinusoidal grating by means of a linear filter model of the detection process , 1989, Perception & psychophysics.

[45]  W. A. van de Grind,et al.  Reaction times to motion onset and motion detection thresholds reflect the properties of bilocal motion detectors , 1989, Vision Research.

[46]  G. Mandl,et al.  Coding for stimulus velocity by temporal patterning of spike discharges in visual cells of cat superior colliculus , 1993, Vision Research.

[47]  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.

[48]  Prrmon Pms LIii,et al.  FACTORS INFLUENCING VELOCITY CODING IN THE HUMAN VISUAL SYSTEM , 2002 .

[49]  S. Mateeff,et al.  The simple reaction time to changes in direction of visual motion , 1999, Experimental Brain Research.

[50]  Aina Puce,et al.  Occipitotemporal Activity Elicited by Viewing Eye Movements: A Magnetoencephalographic Study , 2001, NeuroImage.

[51]  S Vanni,et al.  Visual motion activates V5 in dyslexics , 1997, Neuroreport.

[52]  K. D. Singh,et al.  Localization and functional analysis of human cortical area V5 using magneto-encephalography , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[53]  Y. Okada,et al.  Genesis of MEG signals in a mammalian CNS structure. , 1997, Electroencephalography and clinical neurophysiology.

[54]  Karl J. Friston,et al.  Speed-dependent motion sensitive responses in V5: an fMRI study , 1998, NeuroImage.

[55]  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.

[56]  C. Galletti,et al.  ‘Real-motion’ cells in area V3A of macaque visual cortex , 2004, Experimental Brain Research.

[57]  E. Brenner,et al.  The difference between the perception of absolute and relative motion: a reaction time study , 1994, Vision Research.

[58]  S. Zeki.  Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[59]  O. Braddick,et al.  Brain Areas Sensitive to Coherent Visual Motion , 2001, Perception.

[60]  G. Orban,et al.  Response latencies of visual cells in macaque areas V1, V2 and V5 , 1989, Brain Research.