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Timing of motion representation in the human visual system
Brain Research 790 Ž1998. 195–201
Research report
Timing of motion representation in the human visual system Yoshiki Kaneoke ) , Masahiko Bundou, Ryusuke Kakigi Department of IntegratiÕe Physiology, National Institute for Physiological Sciences, Myodaiji-cho, Okazaki 444, Japan Accepted 13 January 1998
Abstract Visual stimulus in apparent motion evokes a magnetic field from the extrastriate cortex in humans. To investigate what this magnetic field represents, we measured the latencies of the responses in three subjects to the stimuli in apparent motion at various spatial separations. These different latencies were inversely related to the spatial separations of the stimuli Žrange of 74 to 182 ms. and correlated with each subject’s reaction time. The direction of motion affected neither the latency of the magnetic response nor the reaction times. Estimations of the origins of the evoked magnetic fields showed they were always in the same area. In two subjects, the sites were around the meeting point of the ascending limb of the inferior temporal sulcus and the lateral occipital sulcus. In the third subject, the site was in the vicinity of the angular gyrus. The difference between the magnetic response and reaction time was fairly constant Žabout 64 ms. among the subjects. We consider the magnetic response to be related to the generation of a motion image: First, the response clearly corresponded to human reaction times to the same stimuli: Second, the fact that the magnetic response was related to the spatial separations but independent of the direction of motion is not explained if the response is evoked simply by both the onset and offset of the object in the stimulus. Furthermore, individual reaction times were mainly delayed by the speed of the process that generated the motion image. q 1998 Elsevier Science B.V. Keywords: Apparent motion; Human; Motion perception; Reaction time; Visual system
1. Introduction Apparent motion is the perception of the smooth motion of an object that flashes in one place then in another with proper spatial and temporal distance w11x. This image of motion is the product of the human brain because no such motion exists in the visual stimuli presented. Because the single flash of an object does not evoke motion, this perception of apparent motion must be created in the brain after the perception of a second flash. Despite this fact, humans perceive the smooth motion of an object along a path running from the first to the second flash. Where and when is this image of apparent motion created in the brain? Possibly apparent motion is perceived by the same mechanism as real motion because neurons that respond to both motions have been found in the primate MTrV5 w13,15x and because lesion in that area results in a deficit in both types of motion perception w27x. Furthermore, models that detect visual motion usually can be used to explain apparent motion perception w12x. These ) Corresponding [email protected]
author.
Fax: q81-564-52-7913; E- mail:
0006-8993r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved. PII S 0 0 0 6 - 8 9 9 3 Ž 9 8 . 0 0 0 6 3 - 8
facts suggest that the image of motion is created within the striate and the extrastriate cortexes. In a previous magnetoencephalography ŽMEG. study, we found that stimuli in apparent motion evoke a magnetic field from the extrastriate area in humans w9x. The location of this area was around the human MTrV5 for three subjects, whereas that for another subject was in the angular gyrus. Despite differences in the estimated locations among subjects, the areas corresponded to those which evoked responses to the smooth motion stimuli used to activate the human MTrV5 in previous positron emission tomography w5,24x and functional magnetic resonance studies w8,23x. It was not certain, however, to what property in the visual stimuli this magnetic response is related nor whether it corresponds to the perception of apparent motion. The stimulus used to evoke apparent motion consists of only the appearance and disappearance of an object, therefore the response might simply be evoked by the onset and offset of the object. In this study we proposed to answer these questions by comparing the magnetic response latency with the reaction time to the stimuli in apparent motion using various spatial separations. Our findings were reported in part at the 20th Annual Meeting
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of the Japan Neuroscience Society ŽSendai, July 1997. and the 27th Annual Meeting of the Society for Neuroscience ŽNew Orleans, November 1997..
2. Subjects and methods The three healthy right-handed subjects who participated in the study were also S10, S15, and S18 in our previous study w9x. We used these subjects because their cortical areas which responded to both smooth and apparent motion stimuli had already been investigated. The stimulus used to evoke apparent motion was composed of two Frames ŽFig. 1.. In Frame 1, a short white bar Ž0.1 = 2.08. always was shown 1.08 offset from the fixation point. A bar of the same size was presented in Frame 2 but the offset varied from 0.058 to 5.08 that of the bar in Frame 1 and was fixed during a given experimental session. We recorded the magnetic field response from the right hemispheres of the subjects’ brains to random Frame change Žpresented in the left visual field.. We used a 37-channel neuromagnetometer ŽMagnes, BTi. w17x as described previously w9x. Each subject lay on his right side on a bed in a magnetically shielded room and gazed at the fixation point on the screen. Frame 1 or 2 was alternated on the screen. Their presentation times were varied randomly from 2 to 3 seconds at steps of 0.2 s. More than 200 magnetic responses to each frame change Žfrom Frame 1 to 2 and from 2 to 1. were averaged separately and filtered Ž1 to 80 Hz.. The trigger pulse used for the averaging occurred just after the bar was projected. The peak latency
Fig. 1. Schematic illustration of the visual stimulus used to evoke apparent motion. The observer gazed at the small circle Žfixation point, f 0.28 visual angle.. Either Frame 1 or 2 was presented for a few seconds, the time being varied randomly at steps of 0.2 s. The interframe interval was about 15 ms because of synchronization to the flyback time of the computer monitor. In Frame 1, a short white bar Ž2.0=0.18. always was presented 1.08 offset from the fixation point. A bar of the same size was presented in Frame 2 but the offset from the bar in Frame 1 was varied from 0.058 to 5.08, but was fixed during a given experimental session.
Fig. 2. Time courses of averaged magnetic fields from one subject ŽS15.. The waveforms for 37 channels were bunched at the mean DC level. Each trace starts at the onset of change in Frame 1 to 2. Spatial separation of the bar is indicated by the value at the left of each trace. The peak latency of the magnetic response is inversely related to the separation of the bars.
for each response was measured from the magnetic field strength calculated as the root-mean-square ŽRMS. value across the 37 channels. We used six different spatial separations of the bars in Frames 1 and 2 Žvisual angle 0.058, 0.18, 0.28, 1.08, 3.08, and 5.08., and data acquisition was repeated 3 times for each separation. Each subject therefore had 18 Ž6 = 3. MEG measurements. We used the single equivalent current dipole model w21x to estimate the location of the cortical activities that produced the magnetic fields. Criteria for the application of the model were the same as reported previously w9x. The location then was superimposed on the magnetic resonance images of each subject for anatomical investigation. To compare the results with actual human responses, we made two different reaction time studies using the same visual stimuli. The subject sat on a chair with the button in his hand and gazed at the fixation point shown on a computer monitor. In one experiment ŽE1., Frames 1 and 2 were alternated randomly for 3 to 4 s at steps of 0.2 s. The subject needed to respond to the change from Frame 1 to 2 or from Frame 2 to 1 a total of 20 times each. In the other experiment ŽE2., the appearance and disappearance Ž3 to 4 s. of the bar in Frame 1 was alternated. In this case, he needed to respond to the appearance as well as disappearance of the bar as soon as possible. The latency from the trigger pulse Žgiven just after the bar was projected. to the pulse induced by button pushing was defined as the
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Fig. 3. Estimated locations of the equivalent current dipoles for all the stimulus conditions and subjects ŽS10, S15, and S18.. Each coordinate value is the mean of six measurements’ data for each spatial separation. The respective mean plus 2 S.D. of the distance between the mean coordinates and each plot for S10, S15, S18 is 0.5, 0.7, and 1.5 cm.
reaction time. We set the frame presentation time for the reaction time studies one second longer than that for the MEG study to decrease subject fatigue. The subjects performed the E1 experimental session three times for each spatial separation of the bars in Frames 1 and 2 and in the E2 session as well. Reaction times below 100 ms and above 1300 ms were omitted from the analysis.
3. Results All the subjects perceived vivid motion of the bar under all the stimulus conditions used in this study. The magnetic
responses to the apparent motion stimuli for all the spatial separations used were composed of a single component and met the criteria for the application of the single equivalent dipole model w9x. Fig. 2 shows the magnetic responses of subject S15 to stimuli at six varied spatial separations. As indicated, the peak latency of the magnetic responses from 78 to 158 ms was inversely related to the degree of separation. The estimated location of the dipole, however, was always in the same area for each subject ŽFig. 3.; i.e., the subjects’ 95% confidence radii w9x for the estimated location of the dipole were 0.5, 0.7, and 1.5 cm. For two subjects ŽS10 and S15., the locations were around the point at which the ascending limb of the inferior
Fig. 4. Effects of the spatial separations of the bar in Frames 1 and 2 on the reaction times ŽRT. and magnetic responses ŽMEG. of three subjects. Open symbols: latencies of the responses to change from Frame 2 to 1; closed symbols: latencies to change from Frame 1 to 2. For all the subjects there were significant differences in the latencies of both RT and MEG to the spatial separations Ž p - 0.01 from a two-way ANOVA of the latencies in two directions for six spatial separations using SYSTAT.. In contrast, there was no main effect of direction on the latencies of RT and MEG and no interaction between the direction and separation for any of the subjects.
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ms for S10, S15, and S18, respectively; none being significantly different from the reaction times to the apparent motion stimulus at 0.058 separation Ž202 " 29, 214 " 25, 228 " 29 ms, respectively.. In contrast, the subjects responded to the simple disappearance of the bar in Frame 1 with latencies Ž128 " 25, 147 " 18, and 160 " 31 ms. similar to those for the apparent motion stimulus of 5.08 Ž132 " 24, 161 " 43, 178 " 36 ms, respectively.. The difference between the reaction time and magnetic response for each stimulus and subject was fairly constant Žabout 64 ms.. Moreover, there was no effect on the separation of the bars ŽFig. 5. among the subjects although there was a significant difference Ž p s 0.006 by Friedman’s test. in the latencies of the reaction times and magnetic responses.
4. Discussion Fig. 5. Changes in RT and MEG latencies, and their differences ŽRTy MEG. for each spatial separation Ž0.058, 0.18, 0.28, 1.08, 3.08, and 5.08. for three subjects Žsquare: S10, circle: S15, triangle: S18.. Because there was no difference in the latencies of the two directions ŽFrame 1 to 2 or Frame 2 to 1., each RT plot was calculated as the mean value of 120 trials for each spatial separation. Similarly, each MEG plot was calculated as the mean peak latency of six measurements in both directions. The respective standard deviations of the RT and MEG data ranged from 20 to 43 ms and from 2 to 7 ms. There is a clear inverse relation between latency and the separation of RT and MEG, the trends being similar for all the subjects. The RT and MEG latencies per subject differed significantly Ž ps 0.006 for both RT and MEG by Friedman’s test.. In contrast, the difference in these latencies ŽRTyMEG. for each subject did not change, and there was no trend in the changes in the separation of the bars.
temporal sulcus meets the lateral occipital sulcus. The estimated location of the dipole for one subject ŽS18. was in the angular gyrus which also was the location for the smooth motion stimulus Žsee figure 3 in Ref. w9x.. The area in each subject corresponded to the area which evoked the magnetic responses to the smooth motion stimuli created by random dot kinematograms w9x. Fig. 4 shows the reaction time study ŽE1. results for each subject together with the magnetic response latencies. Both the reaction times and magnetic response latencies show a significant inverse relation Ž p - 0.01. to the spatial separation for all the subjects in a two-way ANOVA of the latencies in the two directions for six spatial separations. The differences between the maximum and minimum latencies of the magnetic responses of the three subjects were 68, 80, 67 ms. The direction of motion had no effect on the magnetic and human reaction latencies of any of the subjects, and there was no interaction between the direction and the separation. The subjects’ mean reaction times to the appearance of the bar in Frame 1 were 215 " 31, 215 " 19, and 214 " 18
The stimuli in apparent motion used in this study evoked magnetic fields which were assumed to originate from the localized cortical area. Varying the spatial separation changed the latency of the magnetic response up to 80 ms. The estimated location, however, was always the same for each subject and corresponded to the cortical region which responded to the smooth motion stimulus ŽFig. 3.. These findings provide further evidence of the existence of a localized cortical area outside the striate cortex, which responds to apparent motion stimuli. In two subjects, the locations were considered to be adjacent to the area of the human homologue of MTrV5 because they were estimated as being the point at which the ascending limb of the inferior temporal sulcus meets the lateral occipital sulcus w24x and because the same areas evoked responses to smooth motion stimuli known to activate human MTrV5 w5,8,23,24x. The estimated site in the remaining subject ŽS18. was in the vicinity of the angular gyrus, but the area also responded to smooth motion stimuli. Our findings do not clarify whether the area that responds to apparent motion corresponds anatomically and functionally to the human homologue of monkey MTrV5. Our findings, however, do indicate that the cortical area which responds to the apparent motion stimulus is outside the striate cortex. There are four possible interpretations of the magnetic response data: First, there may merely be a response to the appearance of the bar Žonset response.. Second, there may be merely a response to the disappearance of the bar Žoffset response.. Third, there may be a simple linear summation of the onset and offset responses. Fourth, the response may represent nonlinear interaction of both stimuli. Here we assume that the onset and offset responses occur with different latencies that are related to location in the visual field. We can clearly state that only the fourth
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Fig. 6. Summary of the MEG results and reaction time study. Four different stimulus conditions and the response latencies to these stimuli are indicated by the symbols Ž‘s ’ and ‘) ’.. The apparent motion direction Žarrow. is always from the place where the bar disappeared Žoff. to the place where it appeared Žon.. Evidence 1 indicates that the latencies of the magnetic response and reaction are inversely related to the spatial separation of the bar. Evidence 2 indicates that the latencies are not affected by the direction of the apparent motion of the bar. Although evidence 1 suggests that the location of the onset or offset of the bar causes the difference in latencies, evidence 2 indicates that the location of the appearance or disappearance of the bar does not affect the latencies, only the distance between the bars affects the latencies Žsee Section 4..
interpretation explains both evidences; i.e., latency was inversely related to the spatial separation and latency was not affected by the direction of the motion that followed Žsee also Fig. 6.. The first possibility predicts that the location of the appearance of the bar in the visual field affects the response latency because the latency varied with the spatial separation of the bars Žcompare the response latencies for the two stimuli on the right in Fig. 6.. This contradicts the findings that the direction of the motion did not affect the latency Ževidence 2 in Fig. 6.. The second possibility is negated by the same reasoning Žcompare the latencies for the two stimuli on the left in Fig. 6 and see evidence 2.. The third possibility is that the magnetic response is composed of two deflections and that the latency change is due to the difference in their latencies. In the case of change in Frame 1 to 2, the latency change with spatial separation must be due to latency change in the response to the bar’s onset in Frame 2 because the offset response to the bar in Frame 1 is the same. The responses for the spatial separations of 0.058 and 5.08 ŽFig. 2. clearly indicate that this is not the case. Because there is no overlapping time in these deflections, we can negate the existence of the same offset response to the bar in Frame 1. We therefore conclude that the evoked magnetic field represents responses generated by the nonlinear interaction of both offset and onset stimuli. In other words, the response is not due simply to the appearance or disappearance of the bar nor to the occurrence of two successive independent events such as the disappearance of the bar followed by
the appearance of another bar. We consider the response to be closely related to the perception of motion. The reaction time study findings indicate that our subjects did not simply respond to the disappearance or appearance of the bar. If the response had just been to the appearance of the bar in each Frame, the reaction time to the change from Frame 1 to 2 would become longer as separation increases w18–20x because the location of the bar appearance shifts to the periphery in the visual field, whereas the reaction time to the change from Frame 2 to 1 would be constant. This would contradict the evidence that there was no difference in the reaction times for the two directions ŽFig. 4.. Likewise, the subjects did not merely respond to the disappearance. Results of the reaction time study done on the simple appearance or disappearance of the bar support this idea. The subjects’ reaction times to its appearance were longer than most values for the apparent motion stimuli, and the reaction times to its disappearance were shorter than most values for the apparent motion stimuli. The findings indicate that the subjects did not just detect and respond to the appearance or disappearance of the bar, at least for stimuli with bar separations between 0.058 and 5.08. Therefore, they must have responded to the motion of the bar even though nothing actually moved; i.e., they were not aware of change on the screen until the whole image of motion was generated. This indicates the existence of neural activity representative of the motion image and which is accessible to the motor execution system, as suggested by Crick and Koch w3,4x. We consider that the neural activity in the extrastri-
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ate cortex, which evoked the magnetic field, is a candidate for the neural correlate of this motion image. That is because this response is considered to represent the generation of the motion image Žas discussed above., and it clearly was correlated with the reaction time. Our subjects must have responded to neural activity in their own brains because their reactions were related to motion which did not exist in the external world they saw. Further study, however, is necessary to determine how and to what extent neural activities in this area are uniquely related to motion perception as compared to activities in other brain areas which might not have been detected by MEG. The mechanism of the effect of spatial separation on the latencies of the magnetic responses is not clear, but a difference in anatomical pathways may not explain the results. That is because up to 80 ms the latency changed with the spatial separation, but for each subject the estimated location was always in the same extrastriate cortical area. Possibly the visual information about motion reaches the MTrV5 via different pathways that are dependent on the speed of the object as Ffytche et al. suggested w6x. We could calculate the ‘apparent speed’ in our visual stimuli by using the simple equation: spatial separation divided by the interframe interval Ž15 ms., and use it to investigate whether the latency of the magnetic response related to the anatomical pathways varied with different apparent speeds. The speed ranged from 3.38 to 3338 sy1 when the separation changed from 0.058 to 5.08. Visual information about stimuli with a separation of than 0.18 therefore should arrive at MTrV5 before arriving at the primary visual cortex ŽV1. according to the results by Ffytche et al. w6x because their speeds exceed 68 sy1 . Although the perception of the speed of apparent motion may differ from that of real motion w2x, we consider that the latency change in the magnetic response can not be due simply to a difference in the pathways to MTrV5 because the latency did not change stepwise even when we compared the latencies for separations between 0.058 and 0.18 Žat which the information should take different pathways to reach MTrV5., whereas the latency did change sequentially with the extent of separation between 0.058 and 5.08. Spatial frequency is another possible factor that causes magnetic response latency change because similar tendencies are reported in the recognition times of gray scales with varied spatial frequency w1x. This dependency of the reaction time on the spatial frequency of visual stimuli is related to the magnetic response latency from the occipital lobe w25x. Although the exact origin of the magnetic response in our study is not clear, each subject’s estimated dipole location was outside the striate cortex Žprobably in the human homologue of MTrV5.. Neural activity in this area is not as sensitive to the location in the visual field as is V1 and the secondary ŽV2. visual cortex w14,23x. The response latency change therefore should be due to the speed of information processing within V1rV2 or between V1rV2 and MTrV5 if spatial frequency is the cause of
the latency change. As stated above, differences in the anatomical pathways to reach MTrV5 do not fully explain the variation in the latency. Taking into account the speed of information transfer in the visual system w22x, it is difficult to think of local circuits within the V1rV2 causing a latency difference up to 80 ms. It is noteworthy that the magnetic field recorded from the human brain is considered to represent the spatiotemporal summation of intracellular currents produced by excitatory postsynaptic potentials for more than a million pyramidal neurons w7,16x. Thus, the latency of a magnetic response does not necessarily indicate the fastest arrival time of information, rather it may represent the speed needed to become synchronized for neural activities in a functional group after information arrival. We consider the magnetic response in our study to represent the latency of neurons to become synchronized because it seems impossible that neural circuits can cause an information transfer delay up to 80 ms before that information arrives at MTrV5. The speed at which a group of neurons become synchronized may be determined by the process of bidirectional information exchange w10x that uses reciprocal neural circuits w26x between the primary and extrastriate cortex. The reason is that the neurons in the extrastriate cortex do not seem to have precise information about the space needed to process motion perception, the speed of which varies with the spatial separation. This means that the local neural circuit in the extrastriate can not do this work only with the information it can hold. The extrastriate cortex therefore must communicate with the lower visual corci which hold such information during its neural process for motion perception. Although the latencies of the magnetic responses and the reaction times differed significantly among the subjects ŽFig. 5., the difference between the reaction time and the latency of the magnetic response was the same for all of them. This indicates that the speed of visual motion perception varied more than the speed of motor execution, which may represent the relative complexity of the task for both the visual and motor systems. In our paradigm, the perception of apparent motion may be more complicated for the visual system than is the execution of button-pushing for the motor system. Our study shows that it is possible to independently measure the processing speed of the motor execution system as well as that of the visual system.
Acknowledgements We thank Mr. O. Nagata and Mr. Y. Takeshima for their technical assistance and Dr. M. Kawato, Dr. N. Osaka, and Dr. I. Murakami for their comments, T. Sekiguchi and H. Yamasaki for their help in editing.
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References w1x B.G. Breitmeyer, Simple reaction time as a measure of the temporal response properties of transient and sustained channels, Vis. Res. 15 Ž1975. 1411–1412. w2x E. Castet, Apparent speed of sampled motion, Vis. Res. 35 Ž1995. 1375–1384. w3x F. Crick, C. Koch, Are we aware of neural activity in primary visual cortex?, Nature 375 Ž1995. 121–123. w4x F. Crick, C. Koch, Cortical areas in visual awareness, Nature 377 Ž1995. 294–295. w5x P. Dupont, G.A. Orban, B. De Bruyn, A. Verbruggen, L. Mortelmans, Many areas in the human brain respond to visual motion, J. Neurophysiol. 72 Ž1994. 1420–1424. w6x D.H. Ffytche, C.N. Guy, S. Zeki, The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex, Brain 118 Ž1995. 1375–1394. w7x M. Hamalainen, R. Hari, R.J. IImoniemi, J. Knuutila, O.V. Lounas¨ ¨¨ maa, Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain, Rev. Mod. Phys. 65 Ž1993. 413–497. w8x R.J. Howard, E. Bullmore, M. Brammer, S.C. Williams, J. Mellers, P. Woodruff, A. David, C. Andrew, M. Allin, A. Simmons, T. Cox, Activation of area V5 by visual perception of motion demonstrated with echoplanar MR imaging, Magn. Reson. Imaging 13 Ž1995. 907–909. w9x Y. Kaneoke, M. Bundou, S. Koyama, H. Suzuki, R. Kakigi, Human cortical area responding to stimuli in apparent motion, NeuroReport 8 Ž1997. 677–682. w10x M. Kawato, H. Hayakawa, T. Inui, A forward–inverse optics model of reciprocal connections between visual cortical areas, Network 4 Ž1993. 415–422. w11x P.A. Kolers, M. von Grunau, Shape and color in apparent motion, Vis. Res. 16 Ž1976. 329–335. w12x G. Mather, Computational modelling of motion detectors: responses to two-frame displays, Spatial Vis. 5 Ž1990. 1–14. w13x A. Mikami, W.T. Newsome, R.H. Wurtz, Motion selectivity in macaque visual cortex: I. Mechanisms of direction and speed selectivity in extrastriate area MT, J. Neurophysiol. 55 Ž1986. 1308–1327. w14x A. Mikami, W.T. Newsome, R.H. Wurtz, Motion selectivity in
w15x
w16x
w17x
w18x w19x
w20x w21x w22x
w23x
w24x
w25x
w26x w27x
201
macaque visual cortex: II. Spatiotemporal range of directional interactions in MT and V1, J. Neurophysiol. 55 Ž1986. 1328–1339. W.T. Newsome, A. Mikami, R.H. Wurtz, Motion selectivity in macaque visual cortex: III. Psychophysics and physiology of apparent motion, J. Neurophysiol. 55 Ž1986. 1340–1351. Y.C. Okada, J. Wu, S. Kyuhou, Genesis of MEG signals in a mammalian CNS structure, Electroencephalogr. Clin. Neurophysiol. 103 Ž1997. 474–485. C. Pantev, C. Gallen, S. Hampson, S. Buchanan, D. Sobel, Reproducibility and validity of neuromagnetic source localization using a large array biomagnetometer, Am. J. EEG Technol. 31 Ž1991. 83–101. W.H. Payne, Reaction time as a function of retinal location, Vis. Res. 6 Ž1966. 729–732. A.T. Poffenberger, Reaction time to retinal stimulation with special reference to the time lost in conduction throughout nerve centers, Arch. Psychol. 3 Ž1912. 1–73. J.D. Rains, Signal luminance and position effects in human reaction time, Vis. Res. 3 Ž1963. 239–251. J. Sarvas, Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem, Physiol. Med. Biol. 32 Ž1987. 11–22. S.J. Thorpe, M. Imbert, Biological constraints on connectionist modelling, in: R. Pfeiffer, Z. Schreter, F. Fogelman-Soulie, L. Steels ŽEds.., Connectionism in Perspective, Elsevier, Amsterdam, 1989, pp. 63–92. R.B.H. Tootell, J.B. Reppas, K.K. Kwong, R. Malach, R.T. Born, T.J. Brady, B.R. Rosen, J.W. Belliveau, Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging, J. Neurosci. 15 Ž1995. 3215–3230. J.D. Watson, R. Myers, R.S. Frackowiak, J.V. Hajnal, R.P. Woods, J.C. Mazziotta, S. Shipp, S. Zeki, Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging, Cereb. Cortex 3 Ž1993. 79–94. S.J. Williamson, L. Kaufman, D. Brenner, Latency of the neuromagnetic response of the human visual cortex, Vis. Res. 18 Ž1978. 107–110. S. Zeki, S. Shipp, The functional logic of cortical connections, Nature 335 Ž1988. 311–317. J. Zihl, D. von Cramon, N. Mai, Selective disturbance of movement vision after bilateral brain damage, Brain 106 Ž1983. 313–340.
Research report
Timing of motion representation in the human visual system Yoshiki Kaneoke ) , Masahiko Bundou, Ryusuke Kakigi Department of IntegratiÕe Physiology, National Institute for Physiological Sciences, Myodaiji-cho, Okazaki 444, Japan Accepted 13 January 1998
Abstract Visual stimulus in apparent motion evokes a magnetic field from the extrastriate cortex in humans. To investigate what this magnetic field represents, we measured the latencies of the responses in three subjects to the stimuli in apparent motion at various spatial separations. These different latencies were inversely related to the spatial separations of the stimuli Žrange of 74 to 182 ms. and correlated with each subject’s reaction time. The direction of motion affected neither the latency of the magnetic response nor the reaction times. Estimations of the origins of the evoked magnetic fields showed they were always in the same area. In two subjects, the sites were around the meeting point of the ascending limb of the inferior temporal sulcus and the lateral occipital sulcus. In the third subject, the site was in the vicinity of the angular gyrus. The difference between the magnetic response and reaction time was fairly constant Žabout 64 ms. among the subjects. We consider the magnetic response to be related to the generation of a motion image: First, the response clearly corresponded to human reaction times to the same stimuli: Second, the fact that the magnetic response was related to the spatial separations but independent of the direction of motion is not explained if the response is evoked simply by both the onset and offset of the object in the stimulus. Furthermore, individual reaction times were mainly delayed by the speed of the process that generated the motion image. q 1998 Elsevier Science B.V. Keywords: Apparent motion; Human; Motion perception; Reaction time; Visual system
1. Introduction Apparent motion is the perception of the smooth motion of an object that flashes in one place then in another with proper spatial and temporal distance w11x. This image of motion is the product of the human brain because no such motion exists in the visual stimuli presented. Because the single flash of an object does not evoke motion, this perception of apparent motion must be created in the brain after the perception of a second flash. Despite this fact, humans perceive the smooth motion of an object along a path running from the first to the second flash. Where and when is this image of apparent motion created in the brain? Possibly apparent motion is perceived by the same mechanism as real motion because neurons that respond to both motions have been found in the primate MTrV5 w13,15x and because lesion in that area results in a deficit in both types of motion perception w27x. Furthermore, models that detect visual motion usually can be used to explain apparent motion perception w12x. These ) Corresponding [email protected]
author.
Fax: q81-564-52-7913; E- mail:
0006-8993r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved. PII S 0 0 0 6 - 8 9 9 3 Ž 9 8 . 0 0 0 6 3 - 8
facts suggest that the image of motion is created within the striate and the extrastriate cortexes. In a previous magnetoencephalography ŽMEG. study, we found that stimuli in apparent motion evoke a magnetic field from the extrastriate area in humans w9x. The location of this area was around the human MTrV5 for three subjects, whereas that for another subject was in the angular gyrus. Despite differences in the estimated locations among subjects, the areas corresponded to those which evoked responses to the smooth motion stimuli used to activate the human MTrV5 in previous positron emission tomography w5,24x and functional magnetic resonance studies w8,23x. It was not certain, however, to what property in the visual stimuli this magnetic response is related nor whether it corresponds to the perception of apparent motion. The stimulus used to evoke apparent motion consists of only the appearance and disappearance of an object, therefore the response might simply be evoked by the onset and offset of the object. In this study we proposed to answer these questions by comparing the magnetic response latency with the reaction time to the stimuli in apparent motion using various spatial separations. Our findings were reported in part at the 20th Annual Meeting
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of the Japan Neuroscience Society ŽSendai, July 1997. and the 27th Annual Meeting of the Society for Neuroscience ŽNew Orleans, November 1997..
2. Subjects and methods The three healthy right-handed subjects who participated in the study were also S10, S15, and S18 in our previous study w9x. We used these subjects because their cortical areas which responded to both smooth and apparent motion stimuli had already been investigated. The stimulus used to evoke apparent motion was composed of two Frames ŽFig. 1.. In Frame 1, a short white bar Ž0.1 = 2.08. always was shown 1.08 offset from the fixation point. A bar of the same size was presented in Frame 2 but the offset varied from 0.058 to 5.08 that of the bar in Frame 1 and was fixed during a given experimental session. We recorded the magnetic field response from the right hemispheres of the subjects’ brains to random Frame change Žpresented in the left visual field.. We used a 37-channel neuromagnetometer ŽMagnes, BTi. w17x as described previously w9x. Each subject lay on his right side on a bed in a magnetically shielded room and gazed at the fixation point on the screen. Frame 1 or 2 was alternated on the screen. Their presentation times were varied randomly from 2 to 3 seconds at steps of 0.2 s. More than 200 magnetic responses to each frame change Žfrom Frame 1 to 2 and from 2 to 1. were averaged separately and filtered Ž1 to 80 Hz.. The trigger pulse used for the averaging occurred just after the bar was projected. The peak latency
Fig. 1. Schematic illustration of the visual stimulus used to evoke apparent motion. The observer gazed at the small circle Žfixation point, f 0.28 visual angle.. Either Frame 1 or 2 was presented for a few seconds, the time being varied randomly at steps of 0.2 s. The interframe interval was about 15 ms because of synchronization to the flyback time of the computer monitor. In Frame 1, a short white bar Ž2.0=0.18. always was presented 1.08 offset from the fixation point. A bar of the same size was presented in Frame 2 but the offset from the bar in Frame 1 was varied from 0.058 to 5.08, but was fixed during a given experimental session.
Fig. 2. Time courses of averaged magnetic fields from one subject ŽS15.. The waveforms for 37 channels were bunched at the mean DC level. Each trace starts at the onset of change in Frame 1 to 2. Spatial separation of the bar is indicated by the value at the left of each trace. The peak latency of the magnetic response is inversely related to the separation of the bars.
for each response was measured from the magnetic field strength calculated as the root-mean-square ŽRMS. value across the 37 channels. We used six different spatial separations of the bars in Frames 1 and 2 Žvisual angle 0.058, 0.18, 0.28, 1.08, 3.08, and 5.08., and data acquisition was repeated 3 times for each separation. Each subject therefore had 18 Ž6 = 3. MEG measurements. We used the single equivalent current dipole model w21x to estimate the location of the cortical activities that produced the magnetic fields. Criteria for the application of the model were the same as reported previously w9x. The location then was superimposed on the magnetic resonance images of each subject for anatomical investigation. To compare the results with actual human responses, we made two different reaction time studies using the same visual stimuli. The subject sat on a chair with the button in his hand and gazed at the fixation point shown on a computer monitor. In one experiment ŽE1., Frames 1 and 2 were alternated randomly for 3 to 4 s at steps of 0.2 s. The subject needed to respond to the change from Frame 1 to 2 or from Frame 2 to 1 a total of 20 times each. In the other experiment ŽE2., the appearance and disappearance Ž3 to 4 s. of the bar in Frame 1 was alternated. In this case, he needed to respond to the appearance as well as disappearance of the bar as soon as possible. The latency from the trigger pulse Žgiven just after the bar was projected. to the pulse induced by button pushing was defined as the
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Fig. 3. Estimated locations of the equivalent current dipoles for all the stimulus conditions and subjects ŽS10, S15, and S18.. Each coordinate value is the mean of six measurements’ data for each spatial separation. The respective mean plus 2 S.D. of the distance between the mean coordinates and each plot for S10, S15, S18 is 0.5, 0.7, and 1.5 cm.
reaction time. We set the frame presentation time for the reaction time studies one second longer than that for the MEG study to decrease subject fatigue. The subjects performed the E1 experimental session three times for each spatial separation of the bars in Frames 1 and 2 and in the E2 session as well. Reaction times below 100 ms and above 1300 ms were omitted from the analysis.
3. Results All the subjects perceived vivid motion of the bar under all the stimulus conditions used in this study. The magnetic
responses to the apparent motion stimuli for all the spatial separations used were composed of a single component and met the criteria for the application of the single equivalent dipole model w9x. Fig. 2 shows the magnetic responses of subject S15 to stimuli at six varied spatial separations. As indicated, the peak latency of the magnetic responses from 78 to 158 ms was inversely related to the degree of separation. The estimated location of the dipole, however, was always in the same area for each subject ŽFig. 3.; i.e., the subjects’ 95% confidence radii w9x for the estimated location of the dipole were 0.5, 0.7, and 1.5 cm. For two subjects ŽS10 and S15., the locations were around the point at which the ascending limb of the inferior
Fig. 4. Effects of the spatial separations of the bar in Frames 1 and 2 on the reaction times ŽRT. and magnetic responses ŽMEG. of three subjects. Open symbols: latencies of the responses to change from Frame 2 to 1; closed symbols: latencies to change from Frame 1 to 2. For all the subjects there were significant differences in the latencies of both RT and MEG to the spatial separations Ž p - 0.01 from a two-way ANOVA of the latencies in two directions for six spatial separations using SYSTAT.. In contrast, there was no main effect of direction on the latencies of RT and MEG and no interaction between the direction and separation for any of the subjects.
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ms for S10, S15, and S18, respectively; none being significantly different from the reaction times to the apparent motion stimulus at 0.058 separation Ž202 " 29, 214 " 25, 228 " 29 ms, respectively.. In contrast, the subjects responded to the simple disappearance of the bar in Frame 1 with latencies Ž128 " 25, 147 " 18, and 160 " 31 ms. similar to those for the apparent motion stimulus of 5.08 Ž132 " 24, 161 " 43, 178 " 36 ms, respectively.. The difference between the reaction time and magnetic response for each stimulus and subject was fairly constant Žabout 64 ms.. Moreover, there was no effect on the separation of the bars ŽFig. 5. among the subjects although there was a significant difference Ž p s 0.006 by Friedman’s test. in the latencies of the reaction times and magnetic responses.
4. Discussion Fig. 5. Changes in RT and MEG latencies, and their differences ŽRTy MEG. for each spatial separation Ž0.058, 0.18, 0.28, 1.08, 3.08, and 5.08. for three subjects Žsquare: S10, circle: S15, triangle: S18.. Because there was no difference in the latencies of the two directions ŽFrame 1 to 2 or Frame 2 to 1., each RT plot was calculated as the mean value of 120 trials for each spatial separation. Similarly, each MEG plot was calculated as the mean peak latency of six measurements in both directions. The respective standard deviations of the RT and MEG data ranged from 20 to 43 ms and from 2 to 7 ms. There is a clear inverse relation between latency and the separation of RT and MEG, the trends being similar for all the subjects. The RT and MEG latencies per subject differed significantly Ž ps 0.006 for both RT and MEG by Friedman’s test.. In contrast, the difference in these latencies ŽRTyMEG. for each subject did not change, and there was no trend in the changes in the separation of the bars.
temporal sulcus meets the lateral occipital sulcus. The estimated location of the dipole for one subject ŽS18. was in the angular gyrus which also was the location for the smooth motion stimulus Žsee figure 3 in Ref. w9x.. The area in each subject corresponded to the area which evoked the magnetic responses to the smooth motion stimuli created by random dot kinematograms w9x. Fig. 4 shows the reaction time study ŽE1. results for each subject together with the magnetic response latencies. Both the reaction times and magnetic response latencies show a significant inverse relation Ž p - 0.01. to the spatial separation for all the subjects in a two-way ANOVA of the latencies in the two directions for six spatial separations. The differences between the maximum and minimum latencies of the magnetic responses of the three subjects were 68, 80, 67 ms. The direction of motion had no effect on the magnetic and human reaction latencies of any of the subjects, and there was no interaction between the direction and the separation. The subjects’ mean reaction times to the appearance of the bar in Frame 1 were 215 " 31, 215 " 19, and 214 " 18
The stimuli in apparent motion used in this study evoked magnetic fields which were assumed to originate from the localized cortical area. Varying the spatial separation changed the latency of the magnetic response up to 80 ms. The estimated location, however, was always the same for each subject and corresponded to the cortical region which responded to the smooth motion stimulus ŽFig. 3.. These findings provide further evidence of the existence of a localized cortical area outside the striate cortex, which responds to apparent motion stimuli. In two subjects, the locations were considered to be adjacent to the area of the human homologue of MTrV5 because they were estimated as being the point at which the ascending limb of the inferior temporal sulcus meets the lateral occipital sulcus w24x and because the same areas evoked responses to smooth motion stimuli known to activate human MTrV5 w5,8,23,24x. The estimated site in the remaining subject ŽS18. was in the vicinity of the angular gyrus, but the area also responded to smooth motion stimuli. Our findings do not clarify whether the area that responds to apparent motion corresponds anatomically and functionally to the human homologue of monkey MTrV5. Our findings, however, do indicate that the cortical area which responds to the apparent motion stimulus is outside the striate cortex. There are four possible interpretations of the magnetic response data: First, there may merely be a response to the appearance of the bar Žonset response.. Second, there may be merely a response to the disappearance of the bar Žoffset response.. Third, there may be a simple linear summation of the onset and offset responses. Fourth, the response may represent nonlinear interaction of both stimuli. Here we assume that the onset and offset responses occur with different latencies that are related to location in the visual field. We can clearly state that only the fourth
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Fig. 6. Summary of the MEG results and reaction time study. Four different stimulus conditions and the response latencies to these stimuli are indicated by the symbols Ž‘s ’ and ‘) ’.. The apparent motion direction Žarrow. is always from the place where the bar disappeared Žoff. to the place where it appeared Žon.. Evidence 1 indicates that the latencies of the magnetic response and reaction are inversely related to the spatial separation of the bar. Evidence 2 indicates that the latencies are not affected by the direction of the apparent motion of the bar. Although evidence 1 suggests that the location of the onset or offset of the bar causes the difference in latencies, evidence 2 indicates that the location of the appearance or disappearance of the bar does not affect the latencies, only the distance between the bars affects the latencies Žsee Section 4..
interpretation explains both evidences; i.e., latency was inversely related to the spatial separation and latency was not affected by the direction of the motion that followed Žsee also Fig. 6.. The first possibility predicts that the location of the appearance of the bar in the visual field affects the response latency because the latency varied with the spatial separation of the bars Žcompare the response latencies for the two stimuli on the right in Fig. 6.. This contradicts the findings that the direction of the motion did not affect the latency Ževidence 2 in Fig. 6.. The second possibility is negated by the same reasoning Žcompare the latencies for the two stimuli on the left in Fig. 6 and see evidence 2.. The third possibility is that the magnetic response is composed of two deflections and that the latency change is due to the difference in their latencies. In the case of change in Frame 1 to 2, the latency change with spatial separation must be due to latency change in the response to the bar’s onset in Frame 2 because the offset response to the bar in Frame 1 is the same. The responses for the spatial separations of 0.058 and 5.08 ŽFig. 2. clearly indicate that this is not the case. Because there is no overlapping time in these deflections, we can negate the existence of the same offset response to the bar in Frame 1. We therefore conclude that the evoked magnetic field represents responses generated by the nonlinear interaction of both offset and onset stimuli. In other words, the response is not due simply to the appearance or disappearance of the bar nor to the occurrence of two successive independent events such as the disappearance of the bar followed by
the appearance of another bar. We consider the response to be closely related to the perception of motion. The reaction time study findings indicate that our subjects did not simply respond to the disappearance or appearance of the bar. If the response had just been to the appearance of the bar in each Frame, the reaction time to the change from Frame 1 to 2 would become longer as separation increases w18–20x because the location of the bar appearance shifts to the periphery in the visual field, whereas the reaction time to the change from Frame 2 to 1 would be constant. This would contradict the evidence that there was no difference in the reaction times for the two directions ŽFig. 4.. Likewise, the subjects did not merely respond to the disappearance. Results of the reaction time study done on the simple appearance or disappearance of the bar support this idea. The subjects’ reaction times to its appearance were longer than most values for the apparent motion stimuli, and the reaction times to its disappearance were shorter than most values for the apparent motion stimuli. The findings indicate that the subjects did not just detect and respond to the appearance or disappearance of the bar, at least for stimuli with bar separations between 0.058 and 5.08. Therefore, they must have responded to the motion of the bar even though nothing actually moved; i.e., they were not aware of change on the screen until the whole image of motion was generated. This indicates the existence of neural activity representative of the motion image and which is accessible to the motor execution system, as suggested by Crick and Koch w3,4x. We consider that the neural activity in the extrastri-
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ate cortex, which evoked the magnetic field, is a candidate for the neural correlate of this motion image. That is because this response is considered to represent the generation of the motion image Žas discussed above., and it clearly was correlated with the reaction time. Our subjects must have responded to neural activity in their own brains because their reactions were related to motion which did not exist in the external world they saw. Further study, however, is necessary to determine how and to what extent neural activities in this area are uniquely related to motion perception as compared to activities in other brain areas which might not have been detected by MEG. The mechanism of the effect of spatial separation on the latencies of the magnetic responses is not clear, but a difference in anatomical pathways may not explain the results. That is because up to 80 ms the latency changed with the spatial separation, but for each subject the estimated location was always in the same extrastriate cortical area. Possibly the visual information about motion reaches the MTrV5 via different pathways that are dependent on the speed of the object as Ffytche et al. suggested w6x. We could calculate the ‘apparent speed’ in our visual stimuli by using the simple equation: spatial separation divided by the interframe interval Ž15 ms., and use it to investigate whether the latency of the magnetic response related to the anatomical pathways varied with different apparent speeds. The speed ranged from 3.38 to 3338 sy1 when the separation changed from 0.058 to 5.08. Visual information about stimuli with a separation of than 0.18 therefore should arrive at MTrV5 before arriving at the primary visual cortex ŽV1. according to the results by Ffytche et al. w6x because their speeds exceed 68 sy1 . Although the perception of the speed of apparent motion may differ from that of real motion w2x, we consider that the latency change in the magnetic response can not be due simply to a difference in the pathways to MTrV5 because the latency did not change stepwise even when we compared the latencies for separations between 0.058 and 0.18 Žat which the information should take different pathways to reach MTrV5., whereas the latency did change sequentially with the extent of separation between 0.058 and 5.08. Spatial frequency is another possible factor that causes magnetic response latency change because similar tendencies are reported in the recognition times of gray scales with varied spatial frequency w1x. This dependency of the reaction time on the spatial frequency of visual stimuli is related to the magnetic response latency from the occipital lobe w25x. Although the exact origin of the magnetic response in our study is not clear, each subject’s estimated dipole location was outside the striate cortex Žprobably in the human homologue of MTrV5.. Neural activity in this area is not as sensitive to the location in the visual field as is V1 and the secondary ŽV2. visual cortex w14,23x. The response latency change therefore should be due to the speed of information processing within V1rV2 or between V1rV2 and MTrV5 if spatial frequency is the cause of
the latency change. As stated above, differences in the anatomical pathways to reach MTrV5 do not fully explain the variation in the latency. Taking into account the speed of information transfer in the visual system w22x, it is difficult to think of local circuits within the V1rV2 causing a latency difference up to 80 ms. It is noteworthy that the magnetic field recorded from the human brain is considered to represent the spatiotemporal summation of intracellular currents produced by excitatory postsynaptic potentials for more than a million pyramidal neurons w7,16x. Thus, the latency of a magnetic response does not necessarily indicate the fastest arrival time of information, rather it may represent the speed needed to become synchronized for neural activities in a functional group after information arrival. We consider the magnetic response in our study to represent the latency of neurons to become synchronized because it seems impossible that neural circuits can cause an information transfer delay up to 80 ms before that information arrives at MTrV5. The speed at which a group of neurons become synchronized may be determined by the process of bidirectional information exchange w10x that uses reciprocal neural circuits w26x between the primary and extrastriate cortex. The reason is that the neurons in the extrastriate cortex do not seem to have precise information about the space needed to process motion perception, the speed of which varies with the spatial separation. This means that the local neural circuit in the extrastriate can not do this work only with the information it can hold. The extrastriate cortex therefore must communicate with the lower visual corci which hold such information during its neural process for motion perception. Although the latencies of the magnetic responses and the reaction times differed significantly among the subjects ŽFig. 5., the difference between the reaction time and the latency of the magnetic response was the same for all of them. This indicates that the speed of visual motion perception varied more than the speed of motor execution, which may represent the relative complexity of the task for both the visual and motor systems. In our paradigm, the perception of apparent motion may be more complicated for the visual system than is the execution of button-pushing for the motor system. Our study shows that it is possible to independently measure the processing speed of the motor execution system as well as that of the visual system.
Acknowledgements We thank Mr. O. Nagata and Mr. Y. Takeshima for their technical assistance and Dr. M. Kawato, Dr. N. Osaka, and Dr. I. Murakami for their comments, T. Sekiguchi and H. Yamasaki for their help in editing.
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References w1x B.G. Breitmeyer, Simple reaction time as a measure of the temporal response properties of transient and sustained channels, Vis. Res. 15 Ž1975. 1411–1412. w2x E. Castet, Apparent speed of sampled motion, Vis. Res. 35 Ž1995. 1375–1384. w3x F. Crick, C. Koch, Are we aware of neural activity in primary visual cortex?, Nature 375 Ž1995. 121–123. w4x F. Crick, C. Koch, Cortical areas in visual awareness, Nature 377 Ž1995. 294–295. w5x P. Dupont, G.A. Orban, B. De Bruyn, A. Verbruggen, L. Mortelmans, Many areas in the human brain respond to visual motion, J. Neurophysiol. 72 Ž1994. 1420–1424. w6x D.H. Ffytche, C.N. Guy, S. Zeki, The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex, Brain 118 Ž1995. 1375–1394. w7x M. Hamalainen, R. Hari, R.J. IImoniemi, J. Knuutila, O.V. Lounas¨ ¨¨ maa, Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain, Rev. Mod. Phys. 65 Ž1993. 413–497. w8x R.J. Howard, E. Bullmore, M. Brammer, S.C. Williams, J. Mellers, P. Woodruff, A. David, C. Andrew, M. Allin, A. Simmons, T. Cox, Activation of area V5 by visual perception of motion demonstrated with echoplanar MR imaging, Magn. Reson. Imaging 13 Ž1995. 907–909. w9x Y. Kaneoke, M. Bundou, S. Koyama, H. Suzuki, R. Kakigi, Human cortical area responding to stimuli in apparent motion, NeuroReport 8 Ž1997. 677–682. w10x M. Kawato, H. Hayakawa, T. Inui, A forward–inverse optics model of reciprocal connections between visual cortical areas, Network 4 Ž1993. 415–422. w11x P.A. Kolers, M. von Grunau, Shape and color in apparent motion, Vis. Res. 16 Ž1976. 329–335. w12x G. Mather, Computational modelling of motion detectors: responses to two-frame displays, Spatial Vis. 5 Ž1990. 1–14. w13x A. Mikami, W.T. Newsome, R.H. Wurtz, Motion selectivity in macaque visual cortex: I. Mechanisms of direction and speed selectivity in extrastriate area MT, J. Neurophysiol. 55 Ž1986. 1308–1327. w14x A. Mikami, W.T. Newsome, R.H. Wurtz, Motion selectivity in
w15x
w16x
w17x
w18x w19x
w20x w21x w22x
w23x
w24x
w25x
w26x w27x
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macaque visual cortex: II. Spatiotemporal range of directional interactions in MT and V1, J. Neurophysiol. 55 Ž1986. 1328–1339. W.T. Newsome, A. Mikami, R.H. Wurtz, Motion selectivity in macaque visual cortex: III. Psychophysics and physiology of apparent motion, J. Neurophysiol. 55 Ž1986. 1340–1351. Y.C. Okada, J. Wu, S. Kyuhou, Genesis of MEG signals in a mammalian CNS structure, Electroencephalogr. Clin. Neurophysiol. 103 Ž1997. 474–485. C. Pantev, C. Gallen, S. Hampson, S. Buchanan, D. Sobel, Reproducibility and validity of neuromagnetic source localization using a large array biomagnetometer, Am. J. EEG Technol. 31 Ž1991. 83–101. W.H. Payne, Reaction time as a function of retinal location, Vis. Res. 6 Ž1966. 729–732. A.T. Poffenberger, Reaction time to retinal stimulation with special reference to the time lost in conduction throughout nerve centers, Arch. Psychol. 3 Ž1912. 1–73. J.D. Rains, Signal luminance and position effects in human reaction time, Vis. Res. 3 Ž1963. 239–251. J. Sarvas, Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem, Physiol. Med. Biol. 32 Ž1987. 11–22. S.J. Thorpe, M. Imbert, Biological constraints on connectionist modelling, in: R. Pfeiffer, Z. Schreter, F. Fogelman-Soulie, L. Steels ŽEds.., Connectionism in Perspective, Elsevier, Amsterdam, 1989, pp. 63–92. R.B.H. Tootell, J.B. Reppas, K.K. Kwong, R. Malach, R.T. Born, T.J. Brady, B.R. Rosen, J.W. Belliveau, Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging, J. Neurosci. 15 Ž1995. 3215–3230. J.D. Watson, R. Myers, R.S. Frackowiak, J.V. Hajnal, R.P. Woods, J.C. Mazziotta, S. Shipp, S. Zeki, Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging, Cereb. Cortex 3 Ž1993. 79–94. S.J. Williamson, L. Kaufman, D. Brenner, Latency of the neuromagnetic response of the human visual cortex, Vis. Res. 18 Ž1978. 107–110. S. Zeki, S. Shipp, The functional logic of cortical connections, Nature 335 Ž1988. 311–317. J. Zihl, D. von Cramon, N. Mai, Selective disturbance of movement vision after bilateral brain damage, Brain 106 Ž1983. 313–340.