Orientation-selective adaptation to illusory contours in human visual cortex

Abstract

Humans can perceive illusory or subjective contours in the absence of any real physical boundaries. We used an adaptation protocol to look for orientation-selective neural responses to illusory contours defined by phase-shifted abutting line gratings in the human visual cortex. We measured functional magnetic resonance imaging (fMRI) responses to illusory-contour test stimuli after adapting to an illusory-contour adapter stimulus that was oriented parallel or orthogonal to the test stimulus. We found orientation-selective adaptation to illusory contours in early (V1 and V2) and higher-tier visual areas (V3, hV4, VO1, V3A/B, V7, LO1, and LO2). That is, fMRI responses were smaller for test stimuli parallel to the adapter than for test stimuli orthogonal to the adapter. In two control experiments using spatially jittered and phase-randomized stimuli, we demonstrated that this adaptation was not just in response to differences in the distribution of spectral power in the stimuli. Orientation-selective adaptation to illusory contours increased from early to higher-tier visual areas. Thus, both early and higher-tier visual areas contain neurons selective for the orientation of this type of illusory contour.

Figure 1.

A, Example illusory-contour stimulus. Abutting line gratings elicited perception of illusory contours (in this case vertical). B, Example adapter stimulus used in the first control experiment that did not evoke illusory-contour percepts. These stimuli were made by misaligning the inducers, shifting each inducer line parallel to its orientation across the illusory boundaries. C, Example adapter stimulus used in the second control experiment. These stimuli were random-noise patterns with the same power spectrum as the illusory-contour stimuli but with randomized phase spectrum.

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.

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.

Figure 4.

Time course of V1 and LO1 fMRI responses to the test stimuli in the main experiment for an individual observer (observer 1). Onset and duration of adapter and test stimulus are shown by black and gray bars, respectively. Light squares and light curve, Responses to orthogonal test stimuli. Dark circles and dark curve, Responses to parallel test stimuli. Mean responses to adapter stimuli were subtracted from time courses. Error bars indicate SEM across repeated trials (in most cases, smaller than the plot symbols).

Figure 5.

Time courses of fMRI responses, averaged across observers, from the main experiment for visual areas V1, V2, V3, hV4, VO1, V3A/B, V7, LO1, and LO2. Same conventions are used as in Figure 3, except error bars reflect SEM across four observers. Measured responses to orthogonal test stimuli were significantly larger than responses to parallel test stimuli in all of the retinotopic visual areas.

Figure 6.

Response amplitudes, averaged across observers, for all visual areas. A, Main experiment (illusory contour adapter). B, First control experiment (misaligned adapter). C, Second control experiment (phase-scrambled adapter). Light bars, Response amplitudes for orthogonal test stimuli. Dark bars, Response amplitudes for parallel test stimuli. Asterisks indicate a statistically significant difference between group average responses to orthogonal and parallel tests (*p < 0.05; **p < 0.01; ***p < 0.001) (Table 1). Error bars represent SEM across four observers.

Figure 7.

Adaptation indices, averaged across observers, for all visual areas. A, Main experiment (illusory contour adapter). Error bars represent 84% confidence intervals for the mean of the four observers estimated from bootstrap-generated distributions of means in individual observers. Visual areas beyond V2 exhibited significantly larger adaptation indices than area V1 (p < 0.05). B, First control experiment (misaligned adapter). C, Second control experiment (phase-scrambled adapter). None of the adaptation indices are statistically different from zero in either control experiment.

Figure 8.

Psychophysical measurements of orientation-selective adaptation. A, Example psychometric functions (observer 4) for detecting illusory contours after adaptation to parallel (black) or orthogonal (gray) illusory contours. Performance is plotted as a function of the misalignment of the test stimuli (the adapters were not misaligned). The size of the plot symbols corresponds to the number of trials at each test misalignment level. Smooth curves indicate best-fit (maximum-likelihood) psychometric functions. B, Examples of psychometric functions (observer 4) for detecting illusory contours after adaptation to parallel or orthogonal misaligned stimuli. C, Ratios between postadaptation detection thresholds (defined as 75% correct) measured with test stimuli parallel and orthogonal to illusory-contour adapter stimuli (without misalignment) and to misaligned adapter stimuli. Asterisks indicate statistically significant threshold decrement for parallel test stimuli (*p < 0.05). Error bars represent 84% confidence interval for the threshold ratios, estimated from bootstrap-generated distributions of threshold ratios in each individual observer.