Lateralized alpha activity and slow potentials shifts over visual cortex track the time course of both endogenous and exogenous orienting of attention

Abstract

Spatial attention can be oriented endogenously, based on current task goals, or exogenously, triggered by salient events in the environment. Based upon literature demonstrating differences in the time course and neural substrates of each type of attention, these two attention systems are often treated as fundamentally distinct. However, recent studies suggest that rhythmic neural activity in the alpha band (8-13Hz) and slow waves in the event-related potential (ERP) may emerge over occipital cortex following both exogenous and endogenous attention cues. To assess whether these neural changes index a common process of spatial attention, we conducted two within-subject experiments varying the two main dimensions over which endogenous and exogenous attention tasks typically differ: cue informativity (spatially predictive vs. non-predictive) and cue format (centrally vs. peripherally presented). Our data demonstrate that all of these cues elicit lateralized ERPs over parietal-occipital cortex and trigger lateralized decreases in occipital alpha activity prior to a target. Critically, each of these measures precisely tracked the commonly observed time course of each type of attention. These results suggest that visual-cortical enhancement in anticipation of a visual target is a universal process of visualspatial attention, regardless of whether attention was oriented based upon top-down goals or bottom-up salience.

Spatial distance of target locations affects the time course of both endogenous and exogenous attentional deployment.

“…To control for other task factors, such as remembering the feature until response or integrating continuously changing features over time, we added a control condition with no spatial attention shifts and subtracted performance on that task from the attention conditions. Using this continuous feature task, we found that endogenous attention was overall slower relative to exogenous attention, replicating previous research (Rabbit & Müller, 1989;Keefe & Störmer, 2020;Chakravarthi & van Rullen, 2011). Critically, we found that attentional deployment times were dependent on spatial distance for both exogenous and endogenous attention.…”

“…These modes of spatial attention, commonly referred to as endogenous and exogenous attention, respectively, both result in behavioral benefits at the attended location, reflected in faster response times and/or higher accuracy for attended relative to unattended information (Posner, 1980; for a review, see Carrasco, 2011). Neural data has shown that the large-scale brain networks involved in each type of attention are in part overlapping (Peelen, et al, 2004;Serences & Yantis, 2007), and recent results indicate that endogenous and exogenous attention cues can produce similar effects in early visual cortex prior to the onset of a target (Keefe & Störmer, 2020). Thus, there are many similarities in how exogenous and endogenous attention affect behavioral and neural processing.…”

“…However, there are also clear differences and much research has argued for two separate attention systems (e.g., Hahn et al, 2006;Chica, et al, 2013). Perhaps most striking are the differences in their temporal dynamics: exogenous attention is deployed quickly and transiently, while endogenous attention is deployed on a relatively slower time scale (Müller & Rabbit, 1989;Nakayama & Mackeben, 1989;Keefe & Störmer, 2020). These differences in time course have been interpreted as a hallmark distinction between exogenous and endogenous attention (Egeth & Yantis, 1997;Eriksen & Hoffman, 1972;Jonides, 1981;Nakayama & Mackeben, 1989;Posner, 1980).…”

Cross-modal orienting of exogenous attention results in visual-cortical facilitation, not suppression

“…In order to investigate whether cross-modal exogenous attention improved performance on the visual task by facilitating visual processing at the cued location, suppressing visual processing at the uncued location, or both, we examined the ERPs elicited by the peripheral cues relative to the central cues at parietal-occipital electrode sites. In particular, we focused on the time window of the ACOP -an ERP component that has previously been associated with the exogenous orienting of attention (McDonald et al, 2013;Keefe & Störmer, 2020). As this component is based on a relative difference between neural activity across the hemispheres, it is unclear whether it reflects a contralateral positivity, which would be consistent with visualcortical enhancement of the attended location; or an ipsilateral negativity, which would be consistent with visual-cortical suppression of the unattended location; or both.…”

“…The ACOP -usually measured as a contralateral-vs.-ipsilateral ERP component -has been proposed as an index of exogenous attention (McDonald et al, 2013). Thus, based on previous studies on theACOP (McDonald et al., 2013;Keefe & Störmer, 2020), the ERP amplitude was measured between 260-360 ms at four parietal-occipital electrode sites (PO7/PO8/P7/P8) separately for the hemisphere contralateral to the cued location, ipsilateral to the cued location, and over bilateral electrode sites following the central cue. A separate and more exploratory (though preregistered) analysis…”