Sequential sampling of visual objects during sustained attention

In a crowded visual scene, attention must be distributed efficiently and flexibly over time and space to accommodate different contexts. It is well established that selective attention enhances the corresponding neural responses, presumably implying that attention would persistently dwell on the task-relevant item. Meanwhile, recent studies, mostly in divided attentional contexts, suggest that attention does not remain stationary but samples objects alternately over time, suggesting a rhythmic view of attention. However, it remains unknown whether the dynamic mechanism essentially mediates attentional processes at a general level. Importantly, there is also a complete lack of direct neural evidence reflecting whether and how the brain rhythmically samples multiple visual objects during stimulus processing. To address these issues, in this study, we employed electroencephalography (EEG) and a temporal response function (TRF) approach, which can dissociate responses that exclusively represent a single object from the overall neuronal activity, to examine the spatiotemporal characteristics of attention in various attentional contexts. First, attention, which is characterized by inhibitory alpha-band (approximately 10 Hz) activity in TRFs, switches between attended and unattended objects every approximately 200 ms, suggesting a sequential sampling even when attention is required to mostly stay on the attended object. Second, the attentional spatiotemporal pattern is modulated by the task context, such that alpha-mediated switching becomes increasingly prominent as the task requires a more uniform distribution of attention. Finally, the switching pattern correlates with attentional behavioral performance. Our work provides direct neural evidence supporting a generally central role of temporal organization mechanism in attention, such that multiple objects are sequentially sorted according to their priority in attentional contexts. The results suggest that selective attention, in addition to the classically posited attentional “focus,” involves a dynamic mechanism for monitoring all objects outside of the focus. Our findings also suggest that attention implements a space (object)-to-time transformation by acting as a series of concatenating attentional chunks that operate on 1 object at a time.Author summary: In a crowded visual scene, attention must be efficiently and flexibly distributed over time and space to accommodate different contexts in a task. Recent studies have proposed that attention is a dynamic process that organizes copious information temporally. However, how the brain coordinates attention among multiple visual objects and whether this dynamic mechanism mediates attention at a general level remain largely unknown. In this study, we analyze electroencephalography (EEG) recordings during a multi-object selective attention task to extract object-specific neuronal responses. We demonstrate that attention rhythmically switches between visual objects every approximately 200 ms. Furthermore, the spatiotemporal sampling profile of attention adaptively changes in various task contexts and correlates with behavioral performance during attention. Our work provides direct neural evidence supporting the idea that multiple objects are sequentially sorted according to their priority in attentional contexts. The results suggest that attention is intrinsically dynamic, acting as a series of concatenating chunks of attention that operate on 1 object at a time to maintain awareness of the whole scene.