Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans

Abstract

Because of attentional limitations, the human visual system can process for awareness and response only a fraction of the input received. Lesion and functional imaging studies have identified frontal, temporal, and parietal areas as playing a major role in the attentional control of visual processing, but very little is known about how these areas interact to form a dynamic attentional network. We hypothesized that the network communicates by means of neural phase synchronization, and we used magnetoencephalography to study transient long-range interarea phase coupling in a well studied attentionally taxing dual-target task (attentional blink). Our results reveal that communication within the fronto-parieto-temporal attentional network proceeds via transient long-range phase synchronization in the beta band. Changes in synchronization reflect changes in the attentional demands of the task and are directly related to behavioral performance. Thus, we show how attentional limitations arise from the way in which the subsystems of the attentional network interact.

Fig. 1.

TFR for the distractor condition subtracted from the target condition. Time 0 marks the onset of the target. The TFR represents the average across subjects and channels and is displayed in units of standard deviation of the baseline (thresholded at a value of 5). TFRs have been normalized for each frequency before averaging.

Fig. 3.

Classification of stimulus- and target-related connections. (A) SI for one subject for a typical stimulus-related (Left, occipital to posterior parietal left) and a typical target-related (Right, frontal left to posterior parietal right) connection. SI was computed based on sensor groups that are most sensitive to a given region. (B) Autocorrelations were computed for the time course of synchronization for each pair of connections. Connections showing a significant peak at 146 ms were classified as stimulus-related (Left shows an example, to cingulum), and connections showing a significant peak at 292 ms were classified as target-related (see Right for an example, frontal left to frontal right). The dashed line represents the 99% confidence limit computed from 1,000 random permutations of the SI time course. (C) The stimulus-related (Left) and target-related (Right) networks are shown with linewidth coding for the strength of synchronization at 260 ms.

Fig. 2.

Localization of the time-frequency target component displayed in Fig. 1. Functional maps of oscillatory power in the beta band were computed for each subject. The functional maps were spatially normalized by using SPM99, and a permutation analysis with SnPM99 was performed. Only areas with a significance of P < 0.01 (corrected) are shown. The maximum of each ROI is marked and labeled and was used for further computations. A single occipital ROI was used.

Fig. 4.

Mean synchronization (SI) in the target-related network. (A) The no-AB condition (solid line) shows a stronger SI during stimulus presentation than that in the AB condition (dashed line). Zero milliseconds corresponds to the onset of the first target. The beginning of the letter stream ranges from -880 to -580 ms. The SI time courses were smoothed with a Savitzky-Golay filter (polynomial order, 3; frame length, 600) and averaged across all significant connections within the target-related network. (B) SI for the components of five successive stimuli. The x axis specifies time after presentation of the first target. Each point represents the mean SI in a 60-ms window centered at 260 ms after the respective stimulus. Values at 260 ms quantify the network synchronization to the first target, and values at 114 ms represent the network synchronization corresponding to the distractor preceding the first target. Conditions are color-coded (black, no-AB; red, AB; blue, target; green, distractor). The dashed lines mark the extent of SI in trials containing only distractors. Points marked with an asterisk are significantly different from their neighbors at the same position (P < 0.05, Kruskall-Wallis test), whereas points within the same shaded area are not significantly different. Negative values arise from the filtering of the SI time courses.