Spontaneous local variations in ongoing neural activity bias perceptual decisions

Abstract

Neural variability in responding to identical repeated stimuli has been related to trial-by-trial fluctuations in ongoing activity, yet the neural and perceptual consequences of these fluctuations remain poorly understood. Using functional neuroimaging, we recorded brain activity in subjects who reported perceptual decisions on an ambiguous figure, Rubin's vase-faces picture, which was briefly presented at variable intervals of > or = 20 s. Prestimulus activity in the fusiform face area, a cortical region preferentially responding to faces, was higher when subjects subsequently perceived faces instead of the vase. This finding suggests that endogenous variations in prestimulus neuronal activity biased subsequent perceptual inference. Furnishing evidence that evoked sensory responses, we then went on to show that the pre- and poststimulus activity interact in a nonlinear way and the ensuing perceptual decisions depend upon the prestimulus context in which they occur.

Fig. 1.

Experimental paradigm and analysis of percept repetitions. (A) During fMRI, subjects were repeatedly shown Rubin's ambiguous figure followed by a noise mask. In each trial, subjects reported whether they had perceived a vase or faces. (B) Distribution of ISIs across trials. (C) The incidence of repetitions for either percept averaged across all ISIs can very well be approximated by a binomial distribution (goodness-of-fit R² = 0.97, for faces percepts, R² = 0.93, for vase percepts).

Fig. 2.

Peristimulus fMRI signal time courses from right FFA (A) and right LOC (B), averaged across subjects as a function of percept. Significant percept-dependent signal differences were found in the right FFA at time points −1.5 s (t₁₁ = 2.88, P = 0.015), 0 s (t₁₁ = 3.34, P = 0.007), and 6 s (t₁₁ = 2.76, P = 0.019) (two-sided paired t tests). Error bars represent ± SEM. The images show, for a single representative subject, the two main regions of interest identified in the localizer experiment.

Fig. 3.

Time-dependent analysis of activity levels in right FFA. (A) BOLD signal time course averaged across subjects and percepts. The inserted plot shows average choice probabilities (expressed as AUC) for time points t_a, t_b, and t_c. Asterisks mark choice probabilities significantly larger (P < 0.05, two-sided paired t test) than 0.5 in epochs t_b (prestimulus baseline) and t_c (peak response), indicating a relationship between higher activity levels and the perceptual decision for faces (individual data shown in Fig. S3). Note that there is no significant correlation between percept and signal at the earlier time point t_a. (B) Stacked distributions of activity levels at time points t_a, t_b, and t_c with the proportion of trials leading to faces and vase percepts indicated in red and blue, respectively. Distributions of FFA signal at t_a and t_b are very similar, but within this distribution face trials are reshuffled to higher signal intensities only at baseline time point t_b as well as during the evoked response in t_c. Fitted Gaussian distributions are indicated by dashed lines.