Isolating the Neural Substrates of Visually Guided Attention Orienting in Humans

Abstract

The neural processes that enable healthy humans to orient attention to sudden visual events are poorly understood because they are tightly intertwined with purely sensory processes. Here we isolated visually guided orienting activity from sensory activity using event-related potentials (ERPs). By recording ERPs to a lateral stimulus and comparing waveforms obtained under conditions of attention and inattention, we identified an early positive deflection over the ipsilateral visual cortex that was associated with the covert orienting of visual attention to the stimulus. Across five experiments with male and female adult participants, this ipsilateral visual orienting activity (VOA) could be distinguished from purely sensory-evoked activity and from other top-down spatial attention effects. The VOA was linked with behavioral measures of orienting, being significantly larger when the stimulus was detected rapidly than when it was detected more slowly, and its presence was independent of saccadic eye movements toward the targets. The VOA appears to be a specific neural index of the visually guided orienting of attention to a stimulus that appears abruptly in an otherwise uncluttered visual field.SIGNIFICANCE STATEMENT The study of visual attention orienting has been an important impetus for the field of cognitive neuroscience. Seminal reaction-time studies demonstrated that a suddenly appearing visual stimulus attracts attention involuntarily, but the neural processes associated with visually guided attention orienting have been difficult to isolate because they are intertwined with sensory processes that trigger the orienting. Here, we disentangled orienting activity from sensory activity using scalp recordings of event-related electrical activity in the human brain. A specific neural index of visually guided attention orienting was identified. Surprisingly, whereas peripheral sensory stimulation is processed initially and predominantly by the contralateral visual cortex, this electrophysiological index of visual orienting was recorded over the cerebral hemisphere that was ipsilateral to the attention-capturing stimulus.

Keywords: attention; attention capture; covert orienting; event-related potentials; visual orienting activity; visually guided orienting.

Figure 1.

Prototypical ERPs elicited by a visual stimulus appearing abruptly to the left or right side of fixation in an otherwise empty field. By convention, ERPs are collapsed across left and right fields and left and right occipital electrodes to reveal waveforms recorded contralaterally and ipsilaterally with respect to stimulus lateralization. The data are from Luck and Hillyard's (1994a) Experiment 3.

Figure 2.

Experiment 1 methods and results. A, Example trial sequence and stimulus display. B, Grand-average ERPs elicited by the red disk, recorded over the contralateral and ipsilateral occipital scalp (electrodes PO7/PO8) in the attend-periphery condition (left) and the attend-fixation condition (right). The horizontal dashed line indicates −4 µV. Negative voltages are plotted upward. C, Attend-periphery minus attend-fixation difference waveforms recorded contralaterally and ipsilaterally to the disk. The shaded region is centered on the initial positive peak in the ipsilateral waveform and is designated as VOA. D, Topographical voltage map of the attend-periphery minus attend-fixation difference amplitude averaged over the 150–190 ms time window (shaded region in C). E, A single regional source (Talairach coordinates: x = −32.6, y = −76.7, z = −4.2) localized to the ipsilateral lingual gyrus accounted for >90% of scalp-recorded activity in the 150–190 ms modeling interval. The ipsilateral and contralateral cerebral hemispheres correspond to the left and right sides of the image, respectively.

Figure 3.

Experiment 2 methods and results. A, Example trial sequence and stimulus display. B, Grand-averaged occipital ERPs elicited by target displays containing no red line (target absent), a high-salience red line, or a low-salience red line. ERPs elicited by the lateral red lines were isolated by subtracting target-absent ERPs from target-present ERPs. Activity triggered by the display-wide luminance change (including N68 and P106) is evident in target-present and target-absent waveforms but is removed from the difference waveform. C, Topographical maps of the difference waves shown in B. The left and right sides of the head correspond to the ipsilateral and contralateral scalp, respectively.

Figure 4.

Method and results from experiment 3. A, Trial sequence showing the change in background luminance (red line) and notched fixation disk on target display. B, Grand-average occipital ERPs elicited by the target display in the two conditions. C, Attend-periphery minus attend-fixation difference waveforms recorded contralaterally and ipsilaterally with respect to the line. D, Topographical voltage maps of the average attend-periphery minus attend-fixation difference within the 175–275 ms time window.

Figure 5.

Methods and results from experiment 4. A, Example trial sequence. B, Grand-average occipital ERPs elicited by the target display in the two conditions. C, Difference waves created by subtracting the attend-disk condition ERPs from the attend-line condition ERPs. Neural activity associated with putatively “pure” sensory processing, including the early negative peak associated with the display-wide luminance change, is removed from the difference waves, leaving activities associated with task-specific attentional processes. The waveforms reveal VOA (shaded in red) associated with the orienting of attention to the red line. D Ipsilateral minus contralateral difference wave corresponding to the isolated waveforms in C, with 95% CIs (vertical red bars). The vertical dashed line indicates the time point at which VOA reached 50% of its peak amplitude. E, Ipsilateral minus contralateral difference wave from D separately plotted for fast- and slow-response trials based on the median reaction times. F, Activity elicited by unrestrained horizontal saccades to the abrupt-onset line in the attend-line condition. The vertical dashed line indicates the time point at which this saccadic activity reached 50% of its peak amplitude. G, Topographical maps of the VOA. The left and right sides of the heads correspond to the ipsilateral and contralateral scalp, respectively.

Figure 6.

Methods and results from experiment 5. A, Example trial sequence. B, Grand-averaged occipital ERPs elicited by disk-present displays across the two conditions. C, Grand-averaged occipital ERPs elicited by disk-absent displays across the two conditions. D, Difference waves created by subtracting the attend-disk condition ERPs from the attend-line condition ERPs, revealing the VOA (shaded in red). E, Topographical maps of the VOA. The left and right sides of the heads correspond to the ipsilateral and contralateral scalp, respectively. F, Ipsilateral minus contralateral difference waves corresponding to the isolated waveforms in D, with 95% CIs (vertical red bars).