Attentional control: temporal relationships within the fronto-parietal network

Abstract

Selective attention to particular aspects of incoming sensory information is enabled by a network of neural areas that includes frontal cortex, posterior parietal cortex, and, in the visual domain, visual sensory regions. Although progress has been made in understanding the relative contribution of these different regions to the process of visual attentional selection, primarily through studies using neuroimaging, rather little is known about the temporal relationships between these disparate regions. To examine this, participants viewed two rapid serial visual presentation (RSVP) streams of letters positioned to the left and right of fixation point. Before each run, attention was directed to either the left or the right stream. Occasionally, a digit appeared within the attended stream indicating whether attention was to be maintained within the same stream ('hold' condition) or to be shifted to the previously ignored stream ('shift' condition). By titrating the temporal parameters of the time taken to shift attention for each participant using a fine-grained psychophysics paradigm, we measured event-related potentials time-locked to the initiation of spatial shifts of attention. The results revealed that shifts of attention were evident earlier in the response recorded over frontal than over parietal electrodes and, importantly, that the early activity over frontal electrodes was associated with a successful shift of attention. We conclude that frontal areas are engaged early for the purpose of executing an attentional shift, likely triggering a cascade through the fronto-parietal network ultimately, resulting in the attentional modulation of sensory events in posterior cortices.

Figure 1. Stimuli and Task

The visual display contained two streams of letters, each of which could contain a cue and a target. Only one stream was attended at a time, with cues and targets appearing within the attended stream only. Cues indicated whether a spatial shift of attention was required (shift cue, 4) or whether attention was to be maintained in the currently attended stream. Participants pressed a button in response to the target (letter S). Over the course of a behavioral testing session, two parameters were staircaised – target duration and cue-to-target interval.

Figure 2. Behavioral Thresholds

The average behavioral thresholds derived for the gap between a cue and target. The two red bars show the thresholds for left and right shift cues while the two blue bars show the same for hold cues. Note the slightly longer thresholds for right than left cues for both shift and hold cues. Note also the larger thresholds for the shift cues. The error bars in this and all plots indicate the between-subject standard error.

Figure 3. Differences between Shift Hits and Random

Raw ERP timecourses for Shift Hits and Random Letter. The first row shows these timecourses derived from the frontal electrodes, while the second row shows the same derived from the parietal electrodes. The first column shows responses to contralateral stimuli, while the second column shows the responses to ipsilateral stimuli. The red dotted lines show the average behavioral threshold for shift cues (see Figure 2). The black dotted line indicates the first timepoint at which the Shift Hits and Random responses reliably separated in each plot. Note the later separation in parietal than frontal electrodes. Note also that the parietal produces very weak responses to ipsilateral cues and no separation in the responses until well past the behavioral threshold.

Figure 4. Topography and timecourse of differences between Shift Hits and Random

(A) The pattern of results was similar for left and right cues but flipped across hemisphere (see Figure 4B). Therefor, the data have been collapsed over left and right presentations of cues by flipping the identity of electrodes across hemispheres in to increase power and reduce complexity. The Shift cue or Random Letter occurred in the left hemifield (top inset) at time 0 (first topographic plot). The first significant difference between the two conditions occurred in the contralateral frontal electrodes (black arrow) at 146ms (Figure 3), spreading shortly thereafter to the ipsilateral frontal electrodes. The next significant difference emerged in the contralateral parietal electrodes (black arrow) at 246ms (Figure 3), which was before the mean behavioral threshold of 286ms (dashed red line). (B) Plot of the difference between left and right cues in the critical time bins.

Figure 5. Differences between Shift Hits and Hold Hits

Raw ERP timecourses for Shift Hits and Hold Hits. The top plot is derived from frontal electrodes and the bottom from parietal electrodes. The red and blue dotted lines indicate the behavioral thresholds for shift and hold cues, respectively. Note the larger and earlier second component for Hold Hits compared to Shift Hits.

Figure 6. Analysis of the second component of Shift and Hold Hits

Latency and peak response of the second component for Shift and Hold Hits in frontal (top row) and parietal (bottom row) electrodes. The first column shows the latency from stimulus onset to the peak response. The second column depicts the peak response. Note the longer latency in both frontal and parietal electrodes for shift compared to hold hits. Note also the stronger response in frontal electrodes for the shift compared to hold cues.