Shape-specific preparatory activity mediates attention to targets in human visual cortex

Abstract

The mechanisms of attention prioritize sensory input for efficient perceptual processing. Influential theories suggest that attentional biases are mediated via preparatory activation of task-relevant perceptual representations in visual cortex, but the neural evidence for a preparatory coding model of attention remains incomplete. In this experiment, we tested core assumptions underlying a preparatory coding model for attentional bias. Exploiting multivoxel pattern analysis of functional neuroimaging data obtained during a non-spatial attention task, we examined the locus, time-course, and functional significance of shape-specific preparatory attention in the human brain. Following an attentional cue, yet before the onset of a visual target, we observed selective activation of target-specific neural subpopulations within shape-processing visual cortex (lateral occipital complex). Target-specific modulation of baseline activity was sustained throughout the duration of the attention trial and the degree of target specificity that characterized preparatory activation patterns correlated with perceptual performance. We conclude that top-down attention selectively activates target-specific neural codes, providing a competitive bias favoring task-relevant representations over competing representations distributed within the same subregion of visual cortex.

Fig. 1.

The pattern-localizer task identified target-specific neural populations in visual cortex. (A) Participants alternately viewed target stimuli (X or O) presented at the centre of the visual display within a circular aperture of dynamic white noise. Participants monitored the stream of X, or O stimuli for an occasional stimulus presented in a smaller font (12.5% targets, randomly distributed). (B) We first performed pattern analysis to verify that our procedure can extract neural activation patterns specifically associated with the two target stimuli. A searchlight analysis examines each region of cortex (sphere, r = 10 mm): each pattern classifier was trained to discriminate between patterns for “X” or “O” estimated from a subset of training data, and classification performance was assessed on an independent test data set. Classifier output indicated whether the stimulus category of the test data matched the classifier prediction. (C) Left and right lateral views of the rendered cortical surface illustrate above-chance discrimination extending throughout left and right visual cortical areas (corrected for multiple comparisons, P_FDR < 0.001). Shading represents brain areas beyond the field of view of our data acquisition protocol, and gray lines indicate coronal slices shown in (D).

Fig. 2.

Preparatory attention activates target-specific neural populations in visual cortex. (A) Participants were cued to attend for either the letter X or O via auditory tones. Target, and non-target, stimuli were semitransparent (range: 83–90% transparency) letters presented over dynamic visual noise. For illustration only, stimuli are depicted here with relative high visibility (60% transparency). Activation data following the onset of a target, or non-target, stimulus were discarded from all analyses of attentional bias. (B) Classification algorithms were trained on each 10 mm sphere of brain data to discriminate between neural patterns for “X” and “O” stimuli observed during the localizer task, and classification accuracy was tested on the neural responses measured whilst participants attended for each of the target letters. Classifier output indicated the match between perception-discriminative patterns identified in training data from the localizer task and the attention-discriminative patterns observed during the test data from the attention task. (C) Searchlight analyses identified a specific subregion of visual cortex where classifiers trained to discriminate between perceptual states for X or O could also discriminate between the cued attentional states (attend X vs. O; P_FDR < 0.05), corresponding to lateral occipital complex (LOC).

Fig. 3.

Attentional bias in anterior and posterior lateral occipital complex (aLOC/pLOC). (A) Region-of-interest analyses confirmed attentional activation of shape-specific neural patterns in bilateral pLOC and aLOC. (B) Time-course analyses revealed that attentional modulation of target-specific patterns following the onset of the cue stimulus was sustained throughout the duration of the trial. In contrast with the sustained attentional modulation, (C) presentation of target stimuli resulted in a transient activation of target-specific neural populations. (D) The accuracy of the pattern match between template-specific bias observed in the attention task and stimulus-driven perception defined by the pattern-localizer within aLOC was positively correlated with detection accuracy for subsequently presented target stimuli (r = 0.59, P = 0.016), but not within pLOC (P = 0.434). (E) Finally, time-course analysis of the correlation between visual template activation and target detection revealed a stronger relationship during the latter portion of the attention trial. Error bars, ± 1 SEM.