How microsaccades relate to lateralized ERP components of spatial attention: A co-registration study.

Covert shifts of attention that follow the presentation of a cue are associated with lateralized components in the event-related potential (ERP): the "early directing attention negativity" (EDAN) and the "anterior directing attention negativity" (ADAN). Traditionally, these shifts are thought to take place while gaze is fixated and, thus, in the absence of saccades. However, microsaccades of small amplitude (<1°) occur frequently and involuntarily also during fixation and are closely correlated with spatial attention. To investigate potential links between microsaccades and lateralized ERP components, we simultaneously recorded eye movements and ERPs in a spatial cueing task. As a first major result, we show that both the posterior EDAN and the orientation of microsaccades align more strongly with the location of the task-relevant part of the cue stimulus than with the direction of the attention shift indicated by that cue. A coupling between microsaccades and EDAN was also present on the single-trial level: The EDAN was largest when microsaccades were oriented toward the relevant cue, but absent when microsaccades were oriented away from it, suggesting that EDAN and microsaccades are generated by the same neural network, which selects relevant stimuli and orients behavior toward them. As a second major result, we show that small corneoretinal artifacts from microsaccades, which fall below conventional EOG rejection thresholds, contaminate the measurement of the ADAN. After correcting the EEG for microsaccade-related artifacts with an optimized variant of independent component analysis, ADAN was abolished at frontal sites, but a genuine ADAN was still present at central sites. Thus, the combined measurement of microsaccades and lateralized ERPs sheds new light onto cue-elicited shifts of covert attention.

Revising the link between microsaccades and the spatial cueing of voluntary attention.

Microsaccades - i.e., small fixational saccades generated in the superior colliculus (SC) - have been linked to spatial attention. While maintaining fixation, voluntary shifts of covert attention toward peripheral targets result in a sequence of attention-aligned and attention-opposing microsaccades. In most previous studies the direction of the voluntary shift is signaled by a spatial cue (e.g., a leftwards pointing arrow) that presents the most informative part of the cue (e.g., the arrowhead) in the to-be attended visual field. Here we directly investigated the influence of cue position and tested the hypothesis that microsaccades align with cue position rather than with the attention shift. In a spatial cueing task, we presented the task-relevant part of a symmetric cue either in the to-be attended visual field or in the opposite field. As a result, microsaccades were still weakly related to the covert attention shift; however, they were strongly related to the position of the cue even if that required a movement opposite to the cued attention shift. Moreover, if microsaccades aligned with cue position, we observed stronger cueing effects on manual response times. Our interpretation of the data is supported by numerical simulations of a computational model of microsaccade generation that is based on SC properties, where we explain our findings by separate attentional mechanisms for cue localization and the cued attention shift. We conclude that during cueing of voluntary attention, microsaccades are related to both - the overt attentional selection of the task-relevant part of the cue stimulus and the subsequent covert attention shift.

Microsaccade-related brain potentials signal the focus of visuospatial attention.

Covert shifts of visuospatial attention are traditionally assumed to occur in the absence of oculomotor behavior. In contrast, recent behavioral studies have linked attentional cueing effects to the occurrence of microsaccades, small eye movements executed involuntarily during attempted fixation. Here we used a new type of electrophysiological marker to explore the attention-microsaccade relationship, the visual brain activity evoked by the microsaccade itself. By shifting the retinal image, microsaccades frequently elicit neural responses throughout the visual pathway, scalp-recordable in the human EEG as a microsaccade-related potential (mSRP). Although mSRPs contain similar signal components (P1/N1) as traditional visually-evoked potentials (VEPs), it is unknown whether they are also influenced by cognition. Based on established findings that VEPs are amplified for visual inputs at currently attended locations, we expected a selective gain-modulation also for mSRPs. Eye movements and EEG were coregistered in a classic spatial cueing task with an endogenous cue. Replicating behavioral findings, the direction of early microsaccades 200-400ms after cue onset was biased towards the cued side. However, for microsaccades throughout the cue-target interval, mSRPs were systematically enhanced at occipital scalp sites contralateral to the cued hemifield. This attention effect resembled that in a control condition with VEPs and did not interact with the direction of the underlying microsaccade, suggesting that mSRPs reflect the focus of sustained visuospatial attention, which remains fixed at the cued location, despite microsaccades. Microsaccades are not merely an artifact source in the EEG; instead, they are followed by cognitively modulated brain potentials that can serve as non-intrusive electrophysiological probes of attention.