Orientation-Selective Adaptation to Illusory Contours in Human Visual Cortex

Observers and scanning sessions.

Four observers (two male and two female, 27–49 years of age) participated in the main experiment and the first control experiment. Two of the observers (one male and one female) also participated in the second control experiment. Each experiment (main and two control experiments) consisted of two scanning sessions. Observers gave informed consent to participate in accordance with the Helsinki convention and National Institutes of Health guidelines for experiments involving human subjects. The experimental protocol was approved by the New York University Committee on Activities Involving Human Subjects.

Visual stimuli.

Illusory-contour stimuli were presented in an annulus (inner radius, 1.5°; outer radius, 4.9°) around the center of fixation (Fig. 1A). Stimuli were arrays of inducer lines, white diagonal (+45 or −45°) line segments (0.23 arc min wide; 1.4° long, 50% contrast) on a uniform gray background, arranged to form horizontal or vertical abutting line gratings phase shifted by 180°, resulting in the percept of crisp illusory contours between adjacent inducer gratings. The position of each line was jittered by a random amount between ±0.15°, parallel to the orientation of the induced illusory contours. This jitter obscured the regularity of the inducer grating pattern, which might have provided a cue to the orientation of the illusory contours even in the absence of an illusory-contour percept. The spatial frequency of the inducer gratings was 2.8 cycles/° on average (ignoring the jitter). The spatial frequency of illusory contours was 1 contour/°.

In addition to the main experiment, we ran two control experiments that used adapter stimuli [see functional magnetic resonance imaging (fMRI) protocol below] designed to be similar to those in the main experiment but did not induce the perception of illusory contours. The test stimuli in these control experiments were the same illusory-contour stimuli that were used in the main experiment; only the adapter stimuli differed. In the first control experiment, each inducer line was shifted (misaligned), parallel to its orientation, by a random amount raging from −0.55 to 0.55° (Fig. 1B). By misaligning the endpoints of inducer lines, this manipulation eliminated the percept of illusory boundaries between adjacent inducer gratings. As in the main experiment, the orientation of the inducers was either +45 or −45°. In the second control experiment, the adapter stimuli were random-noise patterns generated by randomizing the phase spectrum of the corresponding illusory-contour stimuli (Fig. 1C).

For a separate psychophysical experiment, stimuli were generated with seven levels of misalignment, ranging from no misalignment, as in the main experiment (Fig. 1A), to the misalignment that was used for the first control experiment (Fig. 1B). As in the first control experiment, each inducer line was shifted parallel to its orientation by a random amount drawn from a uniform distribution.

For the fMRI experiments, stimuli were presented on an electromagnetically shielded analog NEC 2110 LCD display using the Psychophysics Toolbox (Brainard, 1997; Pelli, 1997) and a 10-bit graphics card. For the psychophysical experiments, stimuli were presented on a Nokia (Finland) 446 XPro CRT display. Both displays had a refresh rate of 60 Hz and spatial resolution of 800 × 600 pixel. The mean luminance of the display background was 18.14 cd/m² in the fMRI experiments and 51.81 cd/m² in the psychophysical experiments. The viewing distance for both the fMRI and psychophysical experiments was 157.5 cm

fMRI protocol.

We used an event-related fMRI adaptation protocol (Fig. 2) (Engel, 2005; Fang et al., 2005; Gardner et al., 2005; Larsson et al., 2006). In this protocol, observers viewed one illusory-contour stimulus repeatedly (the adapter), and we measured the fMRI response to a subsequently presented illusory-contour stimulus (the test) that had either the same (“parallel”) or perpendicular (“orthogonal”) illusory-contour orientation as the adapter.

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Figure 2.

Experimental protocol. A, Each trial consisted of top-up adaptation followed by a test stimulus. To control and equate attention across trials, observers performed an attention-demanding task at fixation, counting the number of Xs shown in a stream of rapidly presented letters (Z, L, N, T, and X), each presented for 160 ms. The letters were shown throughout each trial, from the beginning of the adapter until the end of presentation of the test stimulus (see Materials and Methods). ISI, Interstimulus interval. B, Schematics of the three trial types. To avoid adaptation to the inducers, the orientation of the inducer lines changed every 160 ms during the adaptation and test period.

At the beginning of each session, observers passively viewed the adapter stimulus for 100 s. Adaptation was maintained on subsequent trials by showing a top-up adapter during the first 4 s of each trial. A blank (uniform gray) screen followed the top-up adapter for 1 s, which was followed by the test stimulus for 1 s. The trial ended with a 1.2 s behavioral-response period, during which the display was blank except for the fixation point (Fig. 2A). Total trial duration was 7.2 s. To avoid adaptation to the inducers (independent of adaptation to the illusory contours), the orientation of the inducers was changed every 160 ms during both the adapter and test stimuli (Fig. 2A) while keeping the illusory-contour orientation constant. In addition, the spatial phase of the illusory contours and that of the inducers was varied randomly every 160 ms.

On one-third of the trials, the test stimulus had the same orientation as the adapter (parallel trials); on one-third, the test stimulus was perpendicular to the adapter (orthogonal trials); and on one-third, the test stimulus was blank (adapter-only trials) (Fig. 2B). The trial order was randomly shuffled so that the sequence of trials preceding and following any trial was equally likely to contain any of the three trial types. Specifically, 14 trials of each trial type were presented in seven blocks of six trials each, with trial order randomized within blocks.

Each observer participated in two scanning sessions, one with a horizontal adapter and the other with a vertical adapter. A single adapter orientation, vertical or horizontal, was used for each scanning session. A scanning session comprised 10 adaptation scans (runs), each consisting of 42 trials (∼5 min), plus two localizer scans (see below). The data were averaged across the two sessions for each observer (i.e., across 840 trials).

To control attention, observers performed an attention-demanding task at fixation (Fig. 2A) that forced them to divert their attention away from the peripheral illusory-contour stimuli. This was necessary, because spatial attention can modulate neuronal responses to visual stimuli measured with fMRI in a spatially specific manner (Tootell et al., 1998; Brefczynski and DeYoe, 1999; Gandhi et al., 1999; Kastner et al., 1999; Somers et al., 1999). Furthermore, attention modulates aftereffects, including the motion aftereffect (Chaudhuri, 1990; Lankheet and Verstraten, 1995; Rees et al., 1997), figural aftereffect (Shulman, 1992; Yeh et al., 1996; Suzuki, 2001), tilt aftereffect (Spivey and Spirn, 2000), and illusory-contour tilt aftereffect (Montaser-Kouhsari and Rajimehr, 2004). In our task, observers were required to count the number of Xs in a stream of rapidly (160 ms/letter) presented letters (Z, L, N, T, and X). The letters were shown from the beginning of the adapter until the end of the test stimulus. Afterward, the letters were replaced by a fixation point, cueing observers to respond by pressing one of four keys corresponding to the number of target Xs detected (1–4). Despite the great attentional and working-memory demands of the task, observers' performance after practice was well above chance (Fig. 3). Importantly, there was no difference in performance between the two experimental conditions, indicating that there was no difference in attentional resources devoted to the task between the parallel and orthogonal conditions that could contribute to differences in fMRI responses that we measured. This also indicates that there was no difference in eye position between the conditions, because breaking fixation would have adversely affected performance. Hence, eye movements did not confound the interpretation of our fMRI results.

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Figure 3.

Task performance. The number of targets detected is plotted as a function of number of targets displayed for both the parallel (black) and orthogonal (gray) trials. The dashed line indicates perfect performance. Error bars represent SEM across four observers. A, Main experiment. B, First control experiment.

We ran two control experiments in which the trial sequence, task, and experimental protocol were identical to the main experiment. In the first control experiment, we used the misaligned stimuli (Fig. 1B) as adapters and the same illusory-contour test stimuli as before. These adapter stimuli were visually similar to the illusory-contour adapter stimuli except for the lack of illusory contours. In the second control experiment, the adapter stimuli had identical power spectra as the illusory-contour stimuli, but the phase spectra were randomized (Fig. 1C). The idea behind both manipulations was to ensure that any adaptation effects observed in the main experiment reflected orientation-selective responses to the perceived illusory contours, rather than being a result of incidental features or first-order (luminance contrast) artifacts in the stimuli. As in the main experiment (see above), each observer participated in two scanning sessions for each control experiment, one with a horizontal adapter and the other with a vertical adapter. Each scanning session comprised 10 scans with 42 trials per scan, as in the main experiment.

Localizer scans.

During each scanning session, before and after the adaptation scans, we performed an additional pair of measurements to independently identify the cortical regions responding to the stimuli. The same abutting line-grating illusory-contour stimuli were used as in the main experiment. A block design was used, alternating between 9.6 s blocks of illusory-contour stimuli and 9.6 s blocks of blank (uniform gray) screen. Observers were instructed to maintain their gaze on a fixation mark at the center of the display throughout the scan. Each localizer scan consisted of 13 stimulus-blank alternations.

MRI acquisition.

A Siemens (Erlangen, Germany) Allegra 3T scanner was used to measure the blood oxygenation level-dependent (BOLD) signal (Ogawa et al., 1990) in T2*-weighted images. The scanner was equipped with a four-channel phased-array surface coil covering the back of the head (NM-011 transmit head coil and NMSC-021 receive coil; Nova Medical, Wakefield, MA). A bite bar was used to minimize head motion. Functional data in the adaptation scanning sessions were acquired using the following parameters: repetition time (TR), 1200 ms; echo time (TE), 30 ms; flip angle, 75°; 64 × 64 matrix size; 19 slices oriented perpendicular to the calcarine sulcus; voxel size, 3 × 3 × 3 mm. For the retinotopy measurements (see below), we used the same imaging parameters with the following exceptions: 24 slices and 1500 ms TR. At the beginning of each session, we also acquired anatomical T1-weighted magnetization-prepared rapid-acquisition gradient echo images that covered the same volume as the functional scans but with twice the in-plane resolution (voxel size, 1.5 × 1.5 × 3 mm).

Defining visual area regions of interest.

Nine regions of interest (ROIs) were defined based on retinotopy (V1, V2, V3, V3A/V3B, hV4, V7, LO1, LO2, and VO1). Standard traveling wave methods for retinotopic mapping were used to identify meridian representations corresponding to boundaries between retinotopically organized visual areas (Engel et al., 1994, 1997; Sereno et al., 1995; DeYoe et al., 1996). The retinotopic mapping scans were obtained in scanning sessions separate from the adaptation sessions. The ROIs were drawn on computationally flattened representations (“flat maps”) of the occipital cortex generated from high-resolution T1-weighted anatomy images using the public domain software SurfRelax (Larsson, 2001) (http://www.cma.mgh.harvard.edu/iatr). Areas V1, V2, V3, V3A/V3B, hV4, and V7 have been described extensively in the literature (Wandell et al., 2005). VO1 is a coarsely retinotopic area anterior and lateral to hV4 (Wandell et al., 2005). LO1 and LO2 are two retinotopic areas in the lateral occipital cortex between dorsal V3 and V5/MT+ (Larsson and Heeger, 2006; Larsson et al., 2006).

fMRI data analysis.

The time-series data from each scan were motion corrected within and between scans (Jenkinson et al., 2002). The time series of each voxel was normalized (divided by its mean intensity) to compensate for variations in intensity with distance from the receiver coil and to convert the data from arbitrary image intensity units to percentage signal change.

For the retinotopy and localizer scans, the time-series data from each voxel were high-pass filtered (cutoffs at 0.026 and 0.02 Hz for the retinotopy and localizer scans, respectively) to remove low-frequency noise and drift (Zarahn et al., 1997; Smith et al., 1999) and then were fit with a sinusoid with period equal to that of the stimulus (Bandettini et al., 1993; Engel et al., 1994) yielding both the phase of the best-fit sinusoid and the correlation (technically, coherence) between the best-fit sinusoid and the measured time series. The coherence reflected the signal-to-noise ratio of the evoked responses (Engel et al., 1997), ranging from 0 (no modulation) to 1 (perfect coherence). The best-fit phase measured the temporal delay of the fMRI signal relative to the stimulus cycle. For the retinotopy scans, the phase corresponded to the polar angle and radial components of the retinotopic map. For the localizer experiments, response phase reflected the stimulus condition that evoked the larger response (illusory-contour stimuli or blank field).

Event-related data from the adaptation scans were analyzed separately for each visual area ROI as follows. For each adaptation session, the ROI was restricted to include only those voxels that responded strongly in the localizer scans taken in the same session. Specifically, the ROIs were restricted to include voxels with a response coherence >0.2 and phase between 0 and π, corresponding to stimulus “on” blocks. This ensured that ROIs included only voxels corresponding to visual field locations within the stimulus annulus and reduced intersession variability (Aguirre et al., 1998) by excluding voxels that did not respond strongly to the stimuli. The normalized time courses were averaged across voxels within each ROI. The resulting mean ROI time courses were filtered using a bandpass filter (0.02–0.2 Hz) to remove low-frequency drift and high-frequency noise. Responses to individual trials were extracted from the mean ROI time course by extracting the 16 time points (19.2 s) beginning with the onset of each trial. For each observer, parallel, orthogonal, and blank trials were each pooled across the two scanning sessions (vertical and horizontal adapters). We estimated the response to the adapter stimulus as the mean response for the adapter-only (blank) trials. The mean response to the adapter stimulus was subtracted from the response to each orthogonal and parallel trial, and the resulting time courses were adjusted to a zero baseline by subtracting the mean of the first four time points (corresponding to the time of presentation of the 4 s adapter and the 1 s blank between adapter and test). The peak response amplitudes evoked by the test stimuli (orthogonal or parallel) for each trial were then computed by averaging the two values of the time course around the peak. These two time points, which were the same for all of the ROIs and observers, corresponded to 4.6 and 5.8 s after test stimulus onset (i.e., typical of the peak hemodynamic impulse response). The response amplitudes of individual parallel and orthogonal trials were averaged by trial type to compute the mean response amplitude for each trial type for each visual area ROI. Confidence intervals for mean response amplitudes were calculated for individual observers as the SEM across trials. We estimated the statistical significance of adaptation (i.e., larger response amplitudes to orthogonal than to parallel trials) using a one-tailed t test in individual observers. For group means, we averaged the response amplitudes across the four observers. Confidence intervals for the group amplitude means were computed as the confidence interval pooled across observers (i.e., by taking the square root of the mean squared SEMs of individual observers divided by square root of the number of observers).

We also computed an adaptation index (AI) for each visual area to quantify the difference between the fMRI responses to parallel and orthogonal test stimuli as a result of adaptation in each visual area. The index was calculated as follows: AI = (A_O − A_P)/(|A_O| + |A_P|), where A_P was the mean response amplitude to the parallel stimulus, and A_O was the mean response amplitude to the orthogonal stimulus. This index ranged from −1 to 1. The index was one if adaptation was completely effective, reducing the response to the parallel stimulus to zero. If adaptation was ineffective, so that responses to the parallel and orthogonal stimuli were identical, the index was zero.

For each ROI, the adaptation indices were computed separately for each observer and then averaged. Confidence intervals for adaptation indices were estimated using a bootstrap method (Efron and Tibshirani, 1993). We estimated the underlying distribution of the adaptation indices by resampling the data 1000 times. The response amplitudes from each ROI and each observer were sampled with replacement to yield a resampled data set with the same size as the original data. The resampled adaptation indices were averaged across the four observers, yielding a distribution of 1000 adaptation indices for each ROI. Upper and lower error bounds for the mean adaptation indices were estimated as the 16th and 84th percentiles of the resulting distributions.

Psychophysical protocol.

To verify that the adapter stimuli were behaviorally effective in eliciting adaptation to illusory contours in the main experiment but not in the first control experiment, we measured postadaptation discrimination thresholds to the stimuli with various amounts of misalignment. The stimuli and protocol were similar to those in the fMRI experiments.

Observers performed a two-interval forced-choice task. Two stimuli were displayed in succession. One had the maximum amount of misalignment (0.55°) and the other (the target) had a smaller amount of misalignment. Observers indicated which stimulus was less misaligned (i.e., the stimulus that had the stronger percept of illusory contours). Before each session, observers viewed an adapter stimulus for 100 s. The adapters were either the illusory contours used in the main fMRI experiment or the misaligned adapter stimuli used in the first control experiment. Each trial was 6.6 s long and began by presenting a top-up adapter for 4 s, followed by a blank screen for 0.5 s, followed by two test stimuli for 0.5 s each, separated by an interstimulus interval of 0.5 s. At the end of each trial, observers indicated by key press which interval contained the (less misaligned) illusory-contour target. The misalignment in the target stimulus was varied by two interleaved one-up, two-down staircases (Wetherill and Levitt, 1965). A single experimental session consisted of 10 blocks, each with 20 trials. Target orientation alternated from block to block but was constant within a block. Each observer participated in at least four experimental sessions (one for each combination of adapter type and adapter orientation). The sessions were run on different days to avoid potential confounding effects of long-term adaptation. There were at least 100 trials for each combination of adapter type (illusory contour or misaligned), adapter orientation (horizontal or vertical), and test-stimulus orientation (orthogonal or parallel). Results were pooled across adapter orientations, and psychometric functions were fit to the data using a maximum-likelihood method (Wichmann and Hill, 2001a,b) (http://bootstrap-software.org/psignifit). Discrimination thresholds were defined as the amount of misalignment corresponding to 75% correct responses.