Repetition-induced changes in BOLD response reflect accumulation of neural activity

Abstract

Recent exposure to a stimulus improves performance with subsequent identification of that same stimulus. This ubiquitous, yet simple, memory phenomenon is termed priming and has been linked to another widespread phenomenon called repetition suppression, which is a repetition-induced reduction in human brain activation as measured using fMRI. Here, competing models of the neural basis of repetition suppression were tested empirically. In a backward masking paradigm, we found that effectively masked object stimuli showed repetition enhancement of brain activation instead of suppression. This finding is consistent with an Accumulation model, but is inconsistent with a Suppression model of neural activity. Enhanced activation and the improved behavioral performance usually associated with priming are both explained by a shift in peak latency of the population neural activity elicited during identification.

Figure 1

Suppression model. The right graph illustrates a simulated neural response to a single repeated (gray) and nonrepeated (black), nondegraded stimulus. The left graph illustrates a simulated BOLD response to those same stimuli. Note that the neural activity and BOLD response graphs use different time scales. The primed neural activity is suppressed and produces a smaller BOLD response.

Figure 2

Accumulation model. The right graph illustrates a simulated neural response to a single repeated (gray) and nonrepeated (black), nondegraded stimulus. The left graph illustrates a simulated BOLD response to those same stimuli. Note that the neural activity and BOLD response graphs use different time scales. The primed neural activity is shifted leftward in time and produces a smaller BOLD response.

Figure 3

Backward masking predictions. The right graphs illustrate a simulated neural response to a single repeated (gray) and nonrepeated (black), stimulus embedded in noise and masked. The left graphs illustrate a simulated BOLD response to those same stimuli. Note that the neural activity and BOLD response graphs use different time scales. Termination of activity due to masking produces opposite results in BOLD response for Accumulation and Suppression models.

Figure 4

Lateral occipital complex. Stimuli used in the localizer runs were high‐contrast intact and scrambled images of familiar objects. Brain images show the extent of the acquired functional data and, within that area, the location of group LOC averaged across nine observers (stereotaxic coordinates: x = 39, y = −61, z = 3; x = −39, y = −64, z = −1). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 5

Backward masking results. Stimuli used in the event‐related runs, shown in A, were images of familiar objects presented at three levels of contrast and embedded in Gaussian noise. Half of the images were preexposed during the localizer runs (primed). Stimulus presentation (83 ms) was preceded by a warning fixation cross (800 ms) and followed by the mask stimulus (117 ms), then followed by 8 s of rest. Activation time courses are shown in B for identified (top) and unidentified or effectively masked (bottom) objects. Black lines: nonprimed; gray lines: primed. Error bars are square root of MSE/n. Accumulation predictions for the upper and lower graphs can be found in Figures 2 and 3, respectively.