Orientation selectivity of motion-boundary responses in human visual cortex

Abstract

Motion boundaries (local changes in visual motion direction) arise naturally when objects move relative to an observer. In human visual cortex, neuroimaging studies have identified a region (the kinetic occipital area [KO]) that responds more strongly to motion-boundary stimuli than to transparent-motion stimuli. However, some functional magnetic resonance imaging (fMRI) studies suggest that KO may encompass multiple visual areas and single-unit studies in macaque visual cortex have identified neurons selective for motion-boundary orientation in areas V2, V3, and V4, implying that motion-boundary selectivity may not be restricted to a single area. It is not known whether fMRI responses to motion boundaries are selective for motion-boundary orientation, as would be expected if these responses reflected the population activity of motion-boundary-selective neurons. We used an event-related fMRI adaptation protocol to measure orientation-selective responses to motion boundaries in human visual cortex. On each trial, we measured the response to a probe stimulus presented after an adapter stimulus (a vertical or horizontal motion-boundary grating). The probe stimulus was either a motion-boundary grating oriented parallel or orthogonal to the adapter stimulus or a transparent-motion stimulus. Orientation-selective adaptation for motion boundaries--smaller responses for trials in which test and adapter stimuli were parallel to each other--was observed in multiple extrastriate visual areas. The strongest adaptation, relative to the unadapted responses, was found in V3A, V3B, LO1, LO2, and V7. Most of the visual areas that exhibited orientation-selective adaptation in our data also showed response preference for motion boundaries over transparent motion, indicating that most of the human visual areas previously shown to respond to motion boundaries are also selective for motion-boundary orientation. These results suggest that neurons selective for motion-boundary orientation are distributed across multiple human visual cortical areas and argue against the existence of a single region or area specialized for motion-boundary processing.

Fig. 1.

Experimental design. A: schematic representation of stimulus conditions. Stimuli were presented in an annulus (inner diameter 1.5°; outer diameter 10°) around fixation. White arrows indicate direction of local dot motion; black dotted lines indicate location of motion-defined boundaries (arrows and lines were not present in the actual stimuli and the relative size of dots has been exaggerated for visualization purposes). In parallel trials (PARA), adapter and probe stimuli were motion-defined gratings with the same orientation. In orthogonal trials (ORTHO), adapter and probe stimuli were orthogonal motion-defined gratings. In transparent-motion control trials (TRANS), adapter stimuli were the same as those in ORTHO and PARA, but probe stimuli were transparent-motion patterns with the same local motion components as those of the motion-defined gratings. B: trial structure. On each trial, the adapter stimulus was shown for 4 s, followed after a 1-s interstimulus interval (stimulus annulus replaced by gray background) by the probe stimulus for 1 s. Throughout the experiment and concurrent with the adapter and probe stimuli, subjects performed an attention-demanding counting task at fixation (counting number of target letters “X” in a rapid stream of distractor letters).

Fig. 2.

Event-related time courses (estimated by linear deconvolution and averaged across scanning sessions) for the 4 visual areas showing the greatest absolute difference in response amplitude between parallel and orthogonal probe stimuli. Dark and light bars in the bottom left corner of each panel indicate presentation of adapter and probe stimuli. Error bars (smaller than plot symbols) represent the SE for each time point (computed as the root mean square of the regression SEs across scanning sessions).

Fig. 3.

Probe stimulus response amplitudes for all visual area regions of interest (ROIs). Error bars: SE across scanning sessions. Bold: areas showing significantly greater response amplitudes to the orthogonal motion-boundary gratings than those to parallel motion-boundary gratings (asterisks *) and/or transparent motion (hashes #) (paired t-test across scanning sessions, df = 9, false discovery rate (FDR) corrected for multiple comparisons at α = 0.05).

Fig. 4.

Orientation-selectivity indexes and preference indexes for visual area ROIs with significantly greater response amplitudes to orthogonal probe stimuli than to parallel probe stimuli and/or transparent-motion probes (ROIs in boldface in Table 1 and Fig. 3). Error bars represent 68% confidence intervals (CIs) for the mean index across scanning sessions, estimated using bootstrapping (see methods). Except for the preference index for LO2 and the orientation-selectivity index for VO1, all indexes were significantly greater than zero (bootstrapped 95% CIs >0; P < 0.05, uncorrected for multiple comparisons). n.s., not significant.