Isolating the Neural Substrates of Visually Guided Attention Orienting in Humans

• Published in: The Journal of neuroscience 2022-05, Vol.42 (20), p.4174-4186
• Main Authors: McDonald, John J, Tay, Daniel, Prime, David J, Hillyard, Steven A
• Format: Article
• Language: English
• Subjects: Adult; Attention; Brain Mapping; Cortex (somatosensory); Event-related potentials; Evoked Potentials - physiology; Female; Humans; Male; Photic Stimulation; Reaction Time - physiology; Saccades; Saccadic eye movements; Substrates; Visual cortex; Visual Cortex - physiology; Visual field; Visual fields; Visual perception; Visual stimuli; Waveforms
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.0205-22.2022

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. 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.