Orientation-specific adaptation in human visual cortex

Abstract

Nearly all methods for analyzing and interpreting functional magnetic resonance imaging (fMRI) data assume that the fMRI signal behaves in an approximately linear manner. However, it has been shown that the mean fMRI response to a pair of briefly presented visual stimuli is significantly smaller than would be expected from the response to a single stimulus. This smaller response could be the result of either a nonlinearity in the fMRI signal or neuronal adaptation. We tested the neuronal adaptation hypothesis by measuring the fMRI response to sequential pairs of sinusoidal gratings that had either the same or orthogonal orientation. The adaptation hypothesis predicts that brain areas with orientation-selective neurons should show a more linear response when the stimulus pair is orthogonal than when the pair is identical. Our results show no orientation-specific adaptation effects in primary visual cortex (V1) but increasing effects along the hierarchy of visual areas (V2, V3, and V4V). A psychophysical contrast detection experiment, using similar oriented gratings as adapters, shows evidence of orientation-specific adaptation in the visual system. These results have implications for the interpretation of rapid event-related fMRI experiments, as well as for recently developed methods that use adaptation as a tool to measure the response properties of underlying neuronal subpopulations.

Figure 1.

Stimulus diagram for fMRI experiments. Subjects viewed 1 sec duration counter-phase-modulated gratings either alone or in successive pairs. Stimulus onset asynchronies were (from top to bottom) as follows: 8, 4, 2, and 1.125 sec. A new trial began every 24 sec. The first stimulus could be either vertical or horizontal (data not shown). Pairs had either the same orientation (A) or were oriented orthogonally (B).

Figure 2.

Stimulus diagram for psychophysical experiments. Subjects made a spatial two-alternative forced-choice decision about the location of the target stimulus, which was a small Gabor patch presented either above or below fixation. The test interval containing the Gabor patches followed a 1 sec sinusoidal grating stimulus (identical to that used in the fMRI experiments) with an SOA of 1.125, 2, 4, or 8 sec. Gabors had either the same orientation as the adapting stimulus (A, C) or were orthogonal (B, D). For the SOA of 1.25, a new trail began every 8 sec (A, B). For the other SOAs, trails began every 16 sec (C, D). For these trials, subjects were tested three times for each adapting stimulus, once at each of the SOAs (2, 4, and 8 sec). In all conditions, an auditory beep alerted the subject to the oncoming test stimulus.

Figure 3.

fMRI time courses in V1. Time courses are shown averaged across repetitions and subjects, for the response to a single stimulus alone (diamonds), a pair of same-oriented gratings (squares), and a pair of orthogonal gratings (circles), for each of the SOAs tested (1.125, 2, 4, and 8 sec). Gray vertical bars indicate when the stimuli were presented. Smooth curves through the data are predictions from the best-fitting difference of gamma functions.

Figure 4.

Predicted response to second stimulus in V1. Time courses from Figure 3 after subtracting the response to the single stimulus alone (diamonds) and shifting the response function back in time to account for the SOA. Symbol conventions are as in Figure 3.

Figure 5.

Maximum amplitude of response to the single stimulus alone (horizontal line) and to the response to the second stimulus after subtracting out the first for the same-orientation pair (squares) and orthogonal pair (circles) for responses in areas V1, V2, V3, and V4V as a function of SOA.

Figure 6.

Time-to-peak response (relative to stimulus onset) to the single stimulus alone and to the paired stimuli as a function of SOA in areas V1, V2, V3, and V4V. Symbol conventions are as in Figure 5.

Figure 7.

Psychophysical results. Detection ratio is the ratio of the contrast detection threshold without an adapting stimulus to the threshold after an adapting stimulus. Squares indicate adaptation by the same-oriented grating, and circles indicate adaptation after the orthogonal grating.