 |
INTRODUCTION |
Segregation of figure from ground and the formation of figure contours are fundamental visual processes that can be achieved through the detection of local differences in features (feature contrast) such as color, orientation, disparity, or texture (Cavanagh 1989
; Nothdurft 1993
; Regan 1989
). Single-unit studies have demonstrated receptive field structures that may be involved in detecting local feature contrast. Some directionally selective cells in several visual areas of monkey, for example, have antagonistic surrounds that suppress cell responses when the direction of motion in the surround matches that in the receptive field center (Allman et al. 1985
; Tanaka et al. 1986
). Although motion pathways sometimes are considered part of a dorsal "where" pathway (Ungerleider and Mishkin 1982
), motion contrast defines objects that can be analyzed by a ventral shape pathway (Van Essen et al. 1992
). Cells in macaque inferotemporal cortex respond to objects that have been defined solely by motion contrast (Sary et al. 1993
, 1995
), and inferotemporal lesions impair the retention of discriminations based on motion-defined forms although they do not interfere with the acquisition of new discriminations (Britten et al. 1992
).
Previous studies of motion processing in humans using PET and functional magnetic resonance imaging (fMRI) have found a variety of regions that respond to moving stimuli (Cheng et al. 1995
; Corbetta et al. 1991
; Dupont et al. 1994
; McCarthy et al. 1995
; McKeefry et al. 1997
; Tootell et al. 1995
; Watson et al. 1993
; Zeki et al. 1991
). Several studies (Dupont et al. 1997
; Gulyas et al. 1994
; Orban et al. 1995
; Reppas et al. 1997
) also have presented stimuli in which motion contrast was used to define contours. An initial study by Gulyas et al. (1994)
concentrated on those regions that were enhanced by attending to motion-defined contour, holding the presence of contour relatively constant. Recent studies by Dupont et al. (1997)
and Reppas et al. (1997)
have focused on the sensory activations produced by motion-defined contours. Both studies compared activations from dot fields translating in a single direction with the activations from dot fields in which contrasting directions of motions in contiguous regions produced motion-defined contours.
Strikingly, the activations reported by Dupont et al. (1997)
, using PET, and Reppas et al. (1997)
, using fMRI, were completely nonoverlapping. Dupont et al. reported that motion contours activated an area they described as lateral area 18 or KO, with smaller activations in the right fusiform gyrus, but no medial activations (aside from a relatively weak activation in ventral extrastriate cortex; coordinate =
14,
84,
16). In contrast, Reppas et al. reported no activations on the lateral surface but extensive medial activations in V1, V2, VP, V3, and V3a. This discrepancy may have reflected in part a difference in the stimuli used in each study. Dupont et al. presented motion gratings within a 3° diam aperture, whereas Reppas et al. presented a variety of motion contours within a much larger 26 × 26° field. For the small field conditions of Dupont et al., even the single-direction condition would have produced motion discontinuities in foveal/parafoveal regions due to the absence of motion outside the 3° patch. These small field stimuli probably did not engage the directionally selective suppressive surrounds found in single-unit studies (Allman et al. 1985
; Tanaka et al. 1986
). Therefore, to the extent that cell responses in early visual areas in medial cortex were modulated by these surrounds, Dupont et al. would not have found large differences in activation between the single-direction and motion-contour conditions. A subsequent fMRI study by the same laboratory (Van Oostende et al. 1997
) reported similar results with a 3° stimulus diameter.
The present experiment was conducted before these reports were published and was therefore not explicitly designed to explore the effects of field size. Because the experiment involved relatively large fields (21° diam), however, the field size hypothesis suggests that the results should correspond to those reported by Reppas et al. (1997)
rather than Dupont et al. (1997)
.
 |
METHODS |
The experiment was separated into generate and test phases for purpose of statistical analysis. A group of subjects was tested in the generate phase of the experiment, activated foci related to motion contrast were defined, and these foci then were replicated in a second group of subjects in the test phase of the experiment.
Subjects
Normal human volunteers were recruited from the local population of undergraduate and graduate students, residents, fellows, and staff at the Washington University Undergraduate campus and Medical School and paid for participation. All subjects were strongly right handed as measured by the Edinburgh handedness inventory (Raczkowski et al. 1974
), between the ages of 18 and 35 yr, had normal or corrected to normal visual acuity, and had no significant neurological history. Informed consent was obtained before participation following guidelines approved by the Human Studies Committee (IRB) and the Radioactive Drug Research Committee of Washington University. Thirty subjects participated in the generate and test phase of the experiment. Data was not used from three subjects because of various technical problems, leaving a final sample size of 10 subjects (3 male, 7 female) in the generate phase and 17 subjects (7 male, 10 female) in the test phase.
Apparatus
All emission and transmission measurements were obtained using the Siemens/ECAT 953b positron emission tomograph, which gathers 31 transaxial, contiguous slices with 3.75 mm between the centers of adjacent slices. The septa were retracted during scanning to permit three-dimensional acquisition, which increases sampling efficiency and enables a lower dose of radiation to be administered (Silbersweig et al. 1993
). Visual displays were presented on a color monitor controlled by an AMIGA 3000 computer. Subjects viewed the display from a distance of ~42 cm. The monitor was covered with a black nonreflective cloth to minimize stray reflections, and the monitor surface was masked with a black circular aperture that subtended 21°. This aperture formed an extrinsic contour (Shimojo et al. 1989
) so that moving stimuli appeared to slide under the aperture as they passed from view. All visual displays involved random dot patterns consisting of 3,800 dots (~12% density with 11 dots/deg2), where each dot was a single pixel ~6 × 7 min and pixel luminance was 50 cd/m2. A small fixation cross was present in all displays and fixation was monitored during all scans by electrooculography (EOG).
PET scanning techniques
The PET scanning activation methodology developed at Washington University was used (Fox et al. 1988
; Mintun et al. 1989
). A lateral skull x-ray was taken to verify head alignment and to identify the glabela and inion as markers to locate the position of the transverse plane intersecting the anterior and posterior commissures (Fox et al. 1985
; Talairach and Tournoux 1988
). 15O-labeled water (half-life of 123 s) was used as a blood flow tracer and administered as an intravenous bolus injection. Ten 40-s scans were performed on each subject with each scan spaced ~12 min apart to allow nearly complete decay of the radioactive tracer between scans. For the generate group, each of five conditions (see further text) was conducted twice (for a total of 10 scans), with the subject in each scan positioned to permit sampling of dorsal or ventral brain regions so that the entire brain was scanned for each condition. The generate data were used to select a single head position for subjects in the subsequent test group. After image reconstruction, a fifth order butterworth filter with a cutoff frequency of 0.5 cycles/cm was applied to smooth the images to 14 mm full width at half-maximum (FWHM). As blood-flow increases are known to be a linear function of radiation counts for scans of <1-min duration (Herscovitch et al. 1983
), the remainder of the text refers to changes in tissue radioactivity as changes in blood flow and quantifies the radiation in terms of PET counts.
All PET images were normalized by linear scaling for global blood flow to 1,000 PET counts (Fox et al. 1987
). Each image was transformed into a standardized stereotactic space (Talairach and Tournoux 1988
) in which the voxels measured 2.0 × 2.0 × 2.0 mm. All subtraction pairs were screened for subject movement and scan pairs with obvious movement artifacts were eliminated from further analysis.
Statistical analyses
The reliability of activations were assessed by testing the replicability of activations obtained from a generate group of subjects in an independent test group of subjects. Using a center-of-mass search algorithm (Mintun et al. 1989
), all peaks of blood-flow change within the visual system with a magnitude of
30 PET counts (a higher threshold of 40 PET counts was chosen for subtraction images involving the low-level static dots control to limit the number of foci) were chosen for replication. Candidate peaks were restricted to the visual system to minimize the number of tested activations. For each subject in the test group, a sphere of 7-mm radius was placed around the focus obtained from the generate group and the mean blood-flow change within this region of interest (ROI) was determined. A one-tailed t-test then was performed to determine if the blood-flow change was significantly greater than zero. The test was one-tailed because the sign of the blood flow change in the generate group specified the expected sign of the change in the test group. Multiple observations from a single subject always were averaged so that in all statistical analyses, each subject contributed a single observation.
The replication analysis restricts the tested activations to those that passed a magnitude criteria in the generate group. This procedure may bypass significant activations due to the relatively small sample size of the generate group. Therefore, foci in images formed from the union of the generate and test groups ("generate plus test" data) also were considered significant if they exceeded a z-score threshold of 3.30, corresponding to an uncorrected two-tailed P value of 0.001.
Conditions: generate group
STATIC DOTS.
On each trial, a stationary dot field was presented for 2,300 ms. The dot field then was replaced for 200 ms by a uniform field the luminance of which was equal to the space-averaged luminance of the dot field. A new dot field then was presented, starting the next trial.
PASSIVE UNIDIRECTIONAL SPEED.
On each trial, a stationary dot field was presented for 1,800 ms. The dots then moved as a coherent sheet for 500 ms. Across trials, the dots could move left, right, up, or down and at either 6.8 or 3.4°/s. At the faster speed, dots were shifted 1 pixel each raster cycle (16.7 ms), whereas at the slower speed, dots were shifted 1 pixel every other raster cycle (33.4 ms). The dots then were replaced by a uniform field for 200 ms as in the static dot condition.
ACTIVE UNIDIRECTIONAL SPEED.
The display was identical to the passive unidirectional speed condition, but on each trial, subjects pressed one of two keys to indicate whether the dots moved at the faster or slower speed.
PASSIVE OBLIQUE MOTION GRATING.
A field of static dots was presented for 1,800 ms. An oblique square wave grating formed purely by motion then was presented for 500 ms. The dots in successive segments of the gratings moved in opposite directions at the same speed. Over trials the paired motions defining the grating were left-right and up-down, with the phase of the grating counterbalanced over trials, and the speed of the dots on a single trial was either 3.4 or 6.8°/s. Over trials, the speed and direction of motion at any pixel location in this condition was identical to that in the unidirectional speed conditions. Each bar of the grating subtended 2° and the grating was positioned so that the fixation point bisected the center bar.
ACTIVE OBLIQUE MOTION GRATING.
The display was identical to that in the passive oblique motion grating condition. Subjects pressed one key if the grating had a steep tilt, a second key if the grating had a shallow tilt. Grating angles were chosen in a presession so that performance (reaction time and accuracy) in the motion grating condition was equivalent to performance in the unidirectional speed condition.
Each PET scan was partitioned into three phases, a warm-up phase, just before scan acquisition, that consisted of 10 trials; a 40-s PET phase, during which blood flow data were collected, consisting of 16 trials; and a postphase of 6 trials. In all scans, subjects were instructed to remain fixated on the fixation cross throughout the scan. EOG recordings during each scan indicated that although subjects occasionally made eye movements that exceeded the 1-2° resolution of the equipment, there was no clear relationship with condition. Subjects practiced all conditions in a session before the PET session. The steep and shallow angles for the motion grating were either 16 and 68° or 59 and 23°, depending on which angle pair produced equivalent performance to the speed condition.
Conditions: test group
Test group subjects received a total of 10 scans involving a single head position, permitting several additional conditions to be tested. The 10 scans consisted of the five conditions given to the generate group subjects, an additional static dots control scan, and four new conditions (1 per scan) that were designed to add information concerning the activations found in the generate group data.
PASSIVE PARALLEL MOTION GRATING.
Two distinct motion cues defined the motion gratings: relative motion caused by the opposing motion of dots in successive "bars," and dynamic occlusion caused by the appearance and disappearance of dots at the border of each bar. Sary et al. (1994)
have shown that the relative motion cue can be isolated using a pure shearing stimulus in which the dots in successive bars move in opposing motions, but the direction of motion is parallel to the bars of the grating rather than oblique. The parallel motion condition involved up-down motion pairs that produced vertical gratings and left-right motion pairs that produced horizontal gratings.
PASSIVE BIDIRECTIONAL SPEED.
The motion grating contained dots moving in two directions, but the dots in different directions were segregated spatially. In this condition, the dots in two spatially coextensive dot fields moved in opposite directions [i.e., one-half the dots moved up (or left) and the other one-half moved down (or right)]. The total number of dots in the union of the two fields was the same as in earlier conditions. Perceptually, the fields appeared as two coherent sheets, one sliding over the other.
PASSIVE STATIC DOT GRATING.
A grating produced by luminance information was presented. On each trial, a static dot field was first presented. The luminance of dots in successive bars then was changed in opposite directions (the dots in 1 bar increased in luminance, the dots in the other bar decreased in luminance, keeping the mean luminance constant) to form a static dot grating with a contrast of 59%.
ACTIVE STATIC DOT GRATING.
The display was identical to that in the passive static dot grating condition, but subjects pressed one key if the grating angle was steep or a second key if the grating angle was shallow. The angles of the grating were set for each subject to produce roughly equivalent performance to the motion grating task.
All test subjects received a presession in which they practiced the speed, motion grating, and static grating tasks. To equate the reaction times for the three tasks, angular differences in the static grating task were set at roughly one-half of those in the motion grating task. Subjects also received passive blocks involving the other conditions (bidirectional speed, parallel motion grating, etc.) so that they were familiar with all stimulus conditions.
 |
RESULTS |
Generate group data
The data from the generate group were analyzed to yield foci that were tested for replication in the test group. Three principal subtractions were examined. The first, unidirectional speed minus static dots, isolated activations caused by a uniformly translating dot field, whereas the next two, motion grating minus static dots and motion grating minus unidirectional speed, isolated activations caused by motion contrast.
Perhaps because the orientation and speed judgments involved a simple suprathreshold task, the observed differences within the visual system between the active and passive conditions were small and essentially confined to medial 17/18 activations, which often show differences between active and passive tasks (Shulman et al. 1997
). Data from the active and passive conditions therefore were averaged in both the generate and test groups and will not be presented separately. Four foci from the unidirectional speed minus static dots subtraction, 10 foci from the motion grating minus static dots subtraction and 9 foci from the motion grating minus unidirectional speed subtraction met the selection criteria (foci were located within the visual system and exceeded a threshold magnitude; see METHODS).
Unidirectional speed
Activations produced by a uniform field of translating dots (with static dots as control) were analyzed first. The left columns of Table 1 show the coordinates of foci from the generate group and the P value for the replication of those foci in the test group. An image combining the generate and test groups (generate plus test group) was constructed to give the best estimate of those foci that replicated (right columns of Table 1; Fig. 1, top). Three of the four foci from the generate group replicated in the test group. These foci reflected early visual areas in the lingual gyrus and cuneus, and the right temporal-occipital-parietal junction (an analogous but nonsignificant focus occurred in the left hemisphere and was masked partly by a more dorsal nonsignificantfocus), which is considered the human homologue ofMT/MST in macaques (Cheng et al. 1995
; Corbetta et al. 1991
; Dupont et al. 1994
; McCarthy et al. 1995
; Tootell et al. 1995
; Watson et al. 1993
; Zeki et al. 1991
). Table 1 also shows those foci, isolated by the automated search routine in the generate plus test image, that were not tested during the replication phase but which passed a z-score threshold of 3.30 (see METHODS). This analysis added activations in areas 17/18 and a right superior temporal sulcus focus very similar to that found in earlier studies (Corbetta et al. 1991
; Dupont et al. 1994
).

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| FIG. 1.
Transverse positron emission tomography slices for unidirectional speed minus static dots (top), motion grating minus static dots (middle), and motion grating minus unidirectional speed (bottom). Images reflect data from the generate + test group. Sup. temp. sulcus, superior temporal sulcus; ling. gyrus, lingual gyrus; coll. sulcus, collateral sulcus; 17/18, Brodmann areas 17/18.
|
|
The uniform motion condition therefore activated regions (e.g., medial visual cortex, MT/MST, superior temporal sulcus) similar to those reported in other studies (Cheng et al. 1995
; Corbetta et al. 1991
; Dupont et al. 1994
; McCarthy et al. 1995
; Tootell et al. 1995
; Watson et al. 1993
; Zeki et al. 1991
).
Motion grating
Activations caused by motion contrast were analyzed by subtracting both the static dots and the unidirectional speed condition from the motion grating conditions. Because an initial analysis found no significant differences between the passive parallel and oblique motion grating conditions, these conditions were averaged.
MOTION GRATING MINUS STATIC DOTS.
All 10 foci from the generate group replicated in the test group (left columns, Table 2 and Fig. 1, middle), including activations in area17/18, dorsal cuneus, right temporal-occipital-parietal junction (human MT/MST), regions slightly dorsal to the temporal-occipital-parietal junction in the middle occipital gyrus, right fusiform gyrus, and lingual gyrus. The two lingual gyrus activations in the generate data did not appear as separate foci in the generate plus test data, but merged to form a large central response. Activations that passed the z-score threshold in the generate plus test data (right panel of Table 2) essentially corresponded to the activations found by the replication analysis.
The motion grating therefore significantly activated most of the regions activated by unidirectional motion (but perhaps more strongly) and added regions in both dorsal and ventral extrastriate cortex. These observations were confirmed by a direct comparison of the two conditions.
MOTION GRATING MINUS UNIDIRECTIONAL SPEED.
This subtraction isolates areas that respond specifically to motion contrast or respond more powerfully to motion contrast than unidirectional motion. Replicable activations (Table 3, Fig. 1) were found in areas 17/18, more dorsal areas in the cuneus, the junction of left temporal, parietal, and occipital cortex [MT/MST; there was also some evidence for a below-threshold right hemisphere response (coordinates = 47,
71, 2; z = 2.95; magnitude = 19)], and ventral areas near the lingual gyrus/collateral sulcus. The only activation added by the z-score threshold occurred in the left middle temporal gyrus. No significant activations were found in the reverse subtraction, unidirectional speed minus motion grating. The unidirectional speed condition essentially activated a subset of the regions activated by the motion grating. An analysis of variance (ANOVA) that compared the three motion grating conditions (active and passive oblique, passive parallel), relative to the appropriate speed condition, at the replicated foci found no significant differences between motion grating conditions at any focus.
The motion contrast conditions therefore significantly increased some activations found for the uniform motion conditions in relatively early visual areas (areas 17/18, MT/MST), while adding dorsal areas in the cuneus, and ventral areas near the lingual gyrus/collateral sulcus. The magnitude of activations in these areas (including the nonsignificant activation in right MT/MST) were compared by a one-factor ANOVA over foci. No differences were significant, even when each pairwise comparison was assessed with a t-test. Motion contrast produced statistically equivalent increases in these areas.
Static dot grating
The activations due to luminance contrast were analyzed next. Because the static grating conditions were not conducted in the generate group, foci for replication were chosen from the motion grating minus unidirectional speed subtraction (which should isolate locations related to feature contrast and contour encoding). Table 4 shows those foci that replicated and for which a local maximum in the static dots grating minus static dots subtraction was present within 14 mm (1 FWHM). The motion grating and static dot grating conditions produced very similar activations in areas 17/18 and the left and right dorsal cuneus, whereas the left collateral sulcus activation of the luminance condition was somewhat more medial in the motion condition.
The z-score threshold uncovered additional activations in the right middle temporal gyrus, the lingual gyrus, and the right fusiform gyrus. The right fusiform activation was not an artifact of cerebellar motor activations during the active task (which involved a right hand key press) because the same focus was present when the passive condition was separately analyzed (coordinates = 29,
63,
10; z = 3.63; magnitude = 51). This focus also was present in the motion grating minus static dots condition (see Table 2) but was present to a lesser degree when only the passive condition was considered (coordinates = 31,
63,
10; z = 1.96; magnitude = 26). The closest focus in the unidirectionalspeed condition was shifted into the cerebellum (coordinates = 27,
53,
12; z = 3.94; magnitude = 46), whereas no focus within 15 mm was found in the passive condition. The cerebellar activation, however, was of sufficient magnitude to prevent the isolation of a significant focus in the motion grating minus unidirectional speed subtraction.
These analyses suggest that areas responding to both luminance and motion contrast occur both dorsally (dorsal cuneus) and ventrally (lingual gyrus/collateral sulcus and perhaps right fusiform). Other areas respond more strongly to motion contrast than static luminance contrast (e.g., MT/MST) or may show a stronger response to static luminance contrast (e.g., right fusiform or middle temporal gyrus).
Bidirectional speed
This condition involved a stimulus that contained opposing directions of motion, as in the motion grating conditions, but these motions occurred in superimposed, rather than contiguous, spatial regions and therefore did not produce any contours. Table 5 shows that the foci from the bidirectional speed minus static dots and bidirectional speed minus unidirectional speed (passive) subtractions, which exceeded the z-score threshold, were confined to early visual regions. Although activation was seen at MT/MST (coordinates = 41,
63, 2; z = 3.00; magnitude = 43), it was not sufficient to exceed threshold. The unidirectional speed condition also produced weak activation in this region (see preceding text). The reverse subtraction, unidirectional speed minus bidirectional speed, yielded only one significant activation near the junction of the inferior part of the parietal-occipital sulcus and the most anterior part of the calcarine sulcus (coordinates = 5,
65, 10; z = 3.29; magnitude = 48).
 |
DISCUSSION |
The main results of the study were as follows.
1) Relative to a static dot control, unidirectional motion produced significant activation in areas 17/18, and lateral extrastriate areas, including the right temporal-occipital-parietal junction and right superior temporal sulcus.
2) Motion-defined gratings increased the activation of areas activated by unidirectional motion, except for the superior temporal sulcus (which was unchanged), and added areas in dorsal and ventral extrastriate cortex. Specifically, relative to unidirectional motion, motion-defined gratings produced significant activation in areas 17/18, the leftMT/MST, the bilateral dorsal cuneus, and ventral areas, including bilateral collateral sulcus/lingual gyrus and the left middle temporal gyrus. The activations produced by the motion grating were similar irrespective of whether the grating was specified by relative motion and dynamic occlusion cues or by relative motion (shearing) alone.
3) Relative to a static dot control, the luminance-defined grating produced activation in areas 17/18, the bilateral dorsal cuneus, and ventral areas, including the left collateral sulcus, right fusiform gyrus, and right middle temporalgyrus.
The introduction noted the striking discrepancy between the results reported by Dupont et al. (1997)
and Reppas et al. (1997)
and suggested that the large field conditions of the present experiment might yield results similar to those of Reppas et al. These expectations were largely met with the activations in areas 17/18, dorsal cuneus, and lingual gyrus/collateral sulcus matching those reported by Reppas et al. (1997)
. One important difference, however, was that the present study found clear evidence that MT/MST activation was enhanced by motion contrast.
Areas activated by both unidirectional motion and motion contrast
The current results corresponded well with previous studies in showing that unidirectional motion activates early visual areas in medial cortex (Dupont et al. 1994
; McCarthy et al. 1995
; McKeefry et al. 1997
; Watson et al. 1993
; Zeki et al. 1991
), the superior temporal sulcus (Corbetta et al. 1991
; Dupont et al. 1994
), and the MT/MST (Corbetta et al. 1991
; Dupont et al. 1994
; McCarthy et al. 1995
; McKeefry et al. 1997
; Tootell et al. 1995
; Watson et al. 1993
; Zeki et al. 1991
). Interestingly, motion contrast clearly enhanced activation in both early visual areas and MT/MST but not in the superior temporal sulcus.
We suggest that the increased activation produced by the motion grating in MT/MST and early visual areas (e.g., areas 17/18), were caused by suppressive surrounds outside the classical receptive field. In other words, these activations may not have directly reflected the coding of grating orientation. Studies in the owl monkey suggest that surround inhibition is found in MT (Allman et al. 1985
; Born and Tootell 1992
) as well as areas 17 and 18 (Allman et al. 1987
), and studies in macaque have reported surround inhibition in MT (Lagae et al. 1989
; Raiguel et al. 1995
; Tanaka et al. 1986
; Xiao et al. 1997
). Allman et al. (1985)
found that many cells in owl monkey had antagonistic surrounds that were directionally selective, with greater suppression when the direction of motion of the surround stimulus matched the direction of motion of the stimulus in the classical receptive field. A smaller number of cells had surrounds that were suppressive irrespective of direction of motion, whereas other cells showed no effect of the surround. Tanaka et al. (1986)
and Lagae et al. (1989)
reported qualitatively similar results in macaque. Born and Tootell (1992)
reported a columnar organization of surround cell responses in owl monkey, with cells in some columns showing reduced responses when the surround and center motion matched, whereas cells in other columns showed greater responses for matching than nonmatching motion directions. Cells of this latter type [which Reppas et al. (1997)
termed wide-field cells] were not reported by Tanaka et al. (1986)
or Allman et al. (1985)
. Tanaka et al. (1986)
found only a very small number of cells in MT that responded better to motion of a large field than motion of a single object (these cells were termed Field cells), but the directional selectivity of the "surrounds" of these cells was not reported.
Later studies of surround inhibition in macaque MT (Raiguel et al. 1995
; Xiao et al. 1997
) have focused on the spatial distribution of the surround and have assessed the presence of surround inhibition with stimuli in which both center and surround motion were in the same direction. Although these latter studies reported a high incidence of antagonistic surrounds [e.g., Raiguel et al. (1995)
found that >90% of cells showed surround suppression of
15%, relative to a no-surround control], they did not indicate whether the surrounds were directionally selective or yielded suppressive responses to surround motion in all directions. They may suggest, however, that wide-field cells, which should not have yielded any suppression under these conditions, are not common in macaque MT. The present discussion assumes that cells with directionally selective surround inhibition are more likely to show reduced responses when surround motion matches rather than mismatches the motion in the classical receptive field.
Surround inhibition should produce responses in the motion grating minus unidirectional speed subtraction even in cortical areas, such as MT, that do not show orientation selectivity to motion contours, independent of local dot motion (Marcar et al. 1995
), or do not respond to motion contours that are confined within a cell's receptive field (Snowden et al. 1991
). The equivalent responses in the superior temporal sulcus for gratings and uniform motion suggest that cells in this region may not have directionally selective suppressive surrounds.
McKeefry et al. (1997)
reported that a comparison of PET scans involving coherent motion [a condition in which 0.66° squares (n = 100) all moved in the same direction within a 20 × 26° field] and scans involving incoherent motion (a condition in which different squares moved in different directions) yielded enhanced activations during incoherent motion in areas they identified as V1/V2 and V5 (i.e., MT). They suggested that these enhancements might reflect the operation of suppressive surrounds. Because the incoherently moving stimuli did not produce motion-defined contours, their results are consistent with the hypothesis that the enhanced activations of early visual areas and MT/MST in the present study reflected the engagement of suppressive surrounds rather than the coding of grating orientation.
The present enhancements in early visual areas matched those reported by Reppas et al. (1997)
, but these authors did not report strong activations in MT/MST. Although some activation of MT appears present in their data (e.g., their Fig. 2), the magnitude of the activation was clearly less than for early visual areas. In the present study, the magnitude of the activations in MT/MST and early visual areas were not significantly different. A reviewer noted that in the Reppas et al. (1997)
study, the motion boundaries were present continuously, whereas in the present study, the boundaries were flashed on for 500 ms every 2.5 s. MT/MST activation may have been enhanced by the onset/offset of the boundaries.
Areas activated by motion contrast but not by unidirectional motion
The motion grating condition also activated dorsal regions in the cuneus and ventral regions in the lingual gyrus/collateral sulcus poorly activated by unidirectional motion. DeYoe et al. (1996)
have published retinotopic maps of visual areas that have been transformed into Talairach space. On the basis of these maps, the dorsal cuneus activations roughly correspond to V3/V3a, whereas the ventral activations roughly correspond to V2/VP. Strong activations in these regions also were reported by Reppas et al. (1997)
. Because uniform motion did not significantly activate these areas, they may be involved in segregating the bars of the grating and/or explicitly coding the orientation of the bars. The lingual gyrus/collateral sulcus activations, for example, were close to an area that was enhanced in a previous study when subjects attended to the form or color of an array of moving colored rectangles (Corbetta et al. 1991
). This argument also is supported by the report of McKeefry et al. (1997)
that these areas were not significantly activated by incoherent motion, which does not produce motion boundaries or segmented regions.
It is quite possible that these areas showed weak (rather than null) activations in the unidirectional speed condition that were sufficiently enhanced by motion contrast to reach significance. This issue is difficult to resolve because the nonsignificant activation that was present at these foci (e.g., Fig. 1) in the unidirectional speed condition might have been caused by spread from nearby significant activations. Regardless, the results show that these foci are very sensitive to motion contrast and are at best weakly activated by noncontrast stimuli.
Relationship between luminance- and motion-defined contours
The luminance-defined grating activated similar dorsal areas in the cuneus, while the left collateral sulcus activation was slightly more lateral than that found for the motion grating. Reppas et al. (1997)
also reported that luminance and motion contours produced similar activations in V1, V2, and V3.
The luminance grating also activated a right fusiform location that previously has been identified with shape processing (Buckner et al. 1995
). This activation was clearly present in the passive condition and therefore was not contaminated by motor activations. This focus also occurred in the motion grating minus static dots subtraction, but was present to a lesser degree when only the passive condition was considered. This region therefore responded to both types of feature contrast but more strongly for luminance contrast. Interestingly, Dupont et al. (1997)
also reported that motion-defined gratings activated this region (coordinates = 30,
62,
16).
Activation of area KO
Dupont et al. (1997)
reported that when the luminance grating or uniform motion conditions were subtracted from the motion grating conditions, a region they describe as lateral area 18 or KO was activated (coordinates = 34,
88, 0 and
28,
94,
4). This area was not significantly activated by the motion gratings in the present study nor in Reppas et al. (1997)
. A more recent fMRI study from the same laboratory as Dupont et al. (Van Oostende et al. 1997
) reported that activation of area KO was not significantly affected in three subjects by changes in stimulus diameter of 3, 7, and 14°. In a subtraction of motion grating minus uniform motion, the corresponding percent signal changes in KO for the three stimulus areas were 1.1, 1.33, and 0.76%. Given the large increase in area from a 3 to 14° diam, however, the fall-off in KO activation at the largest diameter is intriguing. With the much larger stimulus areas used in Reppas et al. and the present study [the stimulus areas corresponding to a 14° (Van Oostende et al.), 21° (present study), and 26° (Reppas et al.) diameter are 154, 346, and 531 deg2], the absence of KO activation in the latter two studies still may be explained by field size. Van Oostende et al. do not report how the field size manipulation in their three subjects affected activations in MT/MST or other visual areas, although elsewhere in the paper, they note that a ventral area described as V3A is sensitive to manipulations of stimulus area. Regions in the dorsal cuneus were not described in their paper.
Conclusions
Adding motion contrast to large moving fields enhanced activations in areas 17/18 and MT/MST and added activations in the dorsal cuneus and lingual gyrus/collateral sulcus that were similar to those added by luminance defined contour. Aside from the significant effects of motion contrast in MT/MST, these results largely corresponded with those of Reppas et al. (1997)
, who also used a large field size, but differed from those of Dupont et al. (1997)
, who used a small field size, indicating that effects of motion contrast may heavily depend on field size. This dependence is consistent with the hypothesis that some motion contrast enhancements observed with large field sizes, particularly in early parts of the motion pathway, may reflect the engagement of suppressive surrounds rather than the coding of contour orientation.