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The Spatial Grain of Motion Perception in Human Peripheral Vision SUSAN J vision Res,, Vol. 36, No. 15, pp. 2283–2295,1996 Pergamon Copyright01996 ElsevierScience Ltd. All rights reserved O042-6989(95)O0291-X Printed in Great Britain 0042-6989/96$15.00+ 0.00 The Spatial Grain of Motion Perception in Human Peripheral Vision SUSAN J. GALVIN,* DAVID R. WILLIAMS,TNANCY J. COLETTA~ Received 30 December 1994; in revisedform 2 October 1995 Motion reversal effects (the apparent reversal of the direction of motion of a high frequency sinusoidal grating) have been attributed to aliasing by the cone mosaic IColetta et al. (1990). Vision Research, 30, 1631-1648] and postreceptoral layers [Anderson & Hess (1990). Vision Research, 30, 1507-1515] in human observers. We present data and a new model which suggest that at least two sampling arrays of different densities affect direction discrimination out to 30° eccentricity. The first sampling layer matches anatomical estimates of the cone density. The second sampling layer is too dense to be the parasol cells alone; midget ganglion cells certainly contribute to this task This is further evidence that motion perception is not mediated exclusively by the magnocelhdar stream. Copyright 01996 Elsevier Science Ltd. Motion Aliasing Sampling Periphery Ganglioncells INTRODUCTION and lower temporal frequencies in the parvocellular pathway. Different cortical areas can draw on both the An importantissuecurrentlyunderdebateis the degreeto parvocellular and magnocellular pathways in ways which different features of the visual scene, such as appropriateto their specialization.For example,although colour and motion, are processed independentlyby the area h4T receives relatively more input from the visual system. The idea of parallel pathwaysgrew out of magnocellular pathway, the parvocellular pathway can the discovery of different ganglion cell types in supportmotionperceptionof stimuliin its spatiotemporal mammalian retinas with different stimulus selectivities range (,Merigan et al., 1991). and speeds of transmission (Lennie, 1980). It has been We have used the motionreversaleffect (Colettaet al., suggested that this functional segregation continues 1990)to estimate the minimumspan of motion detectors through cortical processing (Zeki, 1978; Ungerleider & in human vision. Our results show that motion detectors Mishkin, 1982; Livingstone & Hubel, 1988). In this in peripheral vision have spans that are too small to be formulation,the midget retinal ganglion cells, which are explained by the spatial density of neurons in the colour selective and support high spatial resolution but magnocellularpathway, implicating the more numerous transmitinformationrelativelyslowly,form the substrate parvocellularneurons in motion perception. for form perception and project to a temporal cortical Coletta et al. (1990) measured motion reversals stream. The parasol cells, with poorer spatial resolution attributable to aliasing by the cone mosaic out to 25°, but higher transmission rates and temporal sensitivity, while Anderson and Hess (1990) described an effect at would provide the only input to the parietal cortical 40° and beyond which they attributed to aliasing at a stream, where motion is processed and the locations of postreceptoral site. In both of these studies the results objects are coded. were modelledusing a singlesamplingarray. We present On the other hand, the idea that corticalspecializations a new two-stage model of the motion reversal effect reflecta direct continuationof the retinalcell populations which clarifies the roles of cone sampling and post- has been criticized by Merigan and Maunsell (1993). receptoral sampling in producing the phenomenon, and They argue that the retinal specializationis chieflyone of which suggests that both receptoral and post-receptoral spatiotemporal selectivity, with tuning to higher spatial samplingdensitiescan be estimatedfrom motionreversal data. Our new measurementsprovide evidence for both receptoral and postreceptoral aliasing and reveal how * To whom all correspondence should be addressed at: Department of their contributionsdepend on retinal eccentricity. Psychology, University of Otago, P.O. Box 56, Dunedin, New Zealand. T Center for Visual Science, University of Rochester, Rochester, NY METHODS 14627-0270, U.S.A. Apparatus ~ College of Optometry, University of Houston, Houston, TX 77204- 6052, U.S.A. All stimuli were produced by a common-path polar- 2283 2284 S. J. GALVIN elfal. ization interferometerdescribed in detail in Sekiguchiet at 4 Hz based on evidencefrom Colettaet al. (1990) that al. (1993). The device produces an interference fringe the strongest reversals could be obtained near that with the contrast, orientation, spatial frequency, and tem]poralfrequency. We used a two interval forced temporal frequency under computer control. choice procedure. For example, on trials with vertical Eye alignment. A bite-bar was used to stabilize the gratings,the observerindicatedby a buttonpresswhether head. The two beams that formed the fringe on the retina the predominantmotion in the stimulus had been to the were focused in the pupil plane and positioned at the right in the first interval and left in the second, or to the Stiles–Crawfordmaximum. The correct axial alignment left in the first interval and right in the second. No was achieved when either of the beams disappeared feedback was given. Each trial was initiated by the abruptlyif the head was moved horizontallyor vertically, observer’sresponse to the previous trial. If the observer indicating that the beam was meeting the edge of the felt he or she had missed seeing the complete stimulus pupil as a focused spot. The beams were centred on the presentation for some reason, he/she signalled that no Stiles–Crawford maximum by setting the spatial fre- response be recorded on that trial, and the stimuluswas quency to a high value to separate the two beams in the inse:rted later in the sequence. The task was quite pupil plane, defocusingthe field stop to give two discsof fatiguing, especially at the larger eccentricities, and the light on the retina, and then translating the head to observers were encouraged to take rests whenever equalize the intensities of the discs. At 20° eccentricity neecled. and beyond, it was helpful to alternate the two beams The durationof each stimulusintervalwas 2 sec. This when setting their intensities to be equal, as it was included500 msec at both the beginningand end of each difficult to make this judgement with continuously interval during which the contrast of the fringe was presented beams. rampedon and off with a Gaussianenvelope.The interval Fixation. Eccentric viewing was controlledby fixating between the two stimuluspresentationsin each trial was an LED. All observationswere made on the horizontal 500 msec. meridian of the temporal retina of the right eye. The eye Vertical gratings were used with observers ML and was realigned horizontally for each eccentricity, as SG. NC had difficulty seeing the motion of vertical different rotations of the eyeball place the pupil in gratings at the first eccentricity used to test her (40°) so different positions relative to the optical axis of the her trialswere run usinghorizontalgratings.ObserverSG interferometer. also found vertical gratings difficult to see at large eccentricities, so psychometric functions were also Observers obtainedfrom SG at 30 and 40° usinghorizontalgratings. Three observersparticipated.ML is emmetropic;SG’S slightmyopiawas correctedwith a small shiftin the axial RESULTS position of the field stop. NC is more myopic, and a The psychometricfunctionsfor observersNC, ML and –0.75 dioptre spherical lens was positionedbetween the SG :ire shown in Fig. 1. The five panels in each of A, B Maxwellian lens and the eye to enable her to bring the and C show data taken at 5, 10, 20, 30 and 40° on one field stop into focus. Observationswere made with the observer.Each point is the mean percentcorrectbased on right eye. The left eye was patched. 100 trials. The error bars give the standard error across ten sessions. Procedure The resultsshow the same general features seen in the Stimuliwere 100%contrastverticalgratingsdriftingto data collected by Coletta et al. (1990). These are the left or right, or horizontal gratings drifting up and highlightedin Fig. 2, which showsthe data from observer down. Measurementswere made at 5, 10,20,30 and 40° NC at 5° eccentricity.As spatialfrequency increases,the with circularstimulusfieldswith diameters2,3, 6, 10and directionof motion of the gratingsbecomes less distinct, 14°respectively.Field size increasedwith eccentricityto and performancegraduallyfalls to chance (50$%correct). ensure a large number of fringe cycles across the field, At this point, which Coletta et al. called thefirst motion even for the low frequencies required in the periphery. null, there is no dominantdirection of motion.At higher An annulus of incoherentlight with an outer diameter of frequenciesthe dominant direction of motion appears to 14°was positionedto exactly surroundthe stimulusfield be o]ppositeto its true direction;thisis the motionreversal for field sizes less than 14°. This had been found to phenomenon. The first spatial frequency at which improve the visibility of the fringe in previous experi- performance returns to chance after the biggest region ments. of mlotionreversal was called the second motion null by At each eccentricity, each observer was tested with a Coletta et al. Since this is not always the second point of set of 15–20 spatial frequencies (chosen for each
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