Common structure of saccades and microsaccades in visual perception.

We obtain large amounts of external information through our eyes, a process often considered analogous to picture mapping onto a camera lens. However, our eyes are never as still as a camera lens, with saccades occurring between fixations and microsaccades occurring within a fixation. Although saccades are agreed to be functional for information sampling in visual perception, it remains unknown if microsaccades have a similar function when eye movement is restricted. Here, we demonstrated that saccades and microsaccades share common spatiotemporal structures in viewing visual objects. Twenty-seven adults viewed faces and houses in free-viewing and fixation-controlled conditions. Both saccades and microsaccades showed distinctive spatiotemporal patterns between face and house viewing that could be discriminated by pattern classifications. The classifications based on saccades and microsaccades could also be mutually generalized. Importantly, individuals who showed more distinctive saccadic patterns between faces and houses also showed more distinctive microsaccadic patterns. Moreover, saccades and microsaccades showed a higher structure similarity for face viewing than house viewing and a common orienting preference for the eye region over the mouth region. These findings suggested a common oculomotor program that is used to optimize information sampling during visual object perception.

Refixation behavior in naturalistic viewing: Methods, mechanisms, and neural correlates.

When freely viewing a scene, the eyes often return to previously visited locations. By tracking eye movements and coregistering eye movements and EEG, such refixations are shown to have multiple roles: repairing insufficient encoding from precursor fixations, supporting ongoing viewing by resampling relevant locations prioritized by precursor fixations, and aiding the construction of memory representations. All these functions of refixation behavior are understood to be underpinned by three oculomotor and cognitive systems and their associated brain structures. First, immediate saccade planning prior to refixations involves attentional selection of candidate locations to revisit. This process is likely supported by the dorsal attentional network. Second, visual working memory, involved in maintaining task-related information, is likely supported by the visual cortex. Third, higher-order relevance of scene locations, which depends on general knowledge and understanding of scene meaning, is likely supported by the hippocampal memory system. Working together, these structures bring about viewing behavior that balances exploring previously unvisited areas of a scene with exploiting visited areas through refixations.

Planning to revisit: Neural activity in refixation precursors.

Eye tracking studies suggest that refixations-fixations to locations previously visited-serve to recover information lost or missed during earlier exploration of a visual scene. These studies have largely ignored the role of precursor fixations-previous fixations on locations the eyes return to later. We consider the possibility that preparations to return later are already made during precursor fixations. This process would mark precursor fixations as a special category of fixations, that is, distinct in neural activity from other fixation categories such as refixations and fixations to locations visited only once. To capture the neural signals associated with fixation categories, we analyzed electroencephalograms (EEGs) and eye movements recorded simultaneously in a free-viewing contour search task. We developed a methodological pipeline involving regression-based deconvolution modeling, allowing our analyses to account for overlapping EEG responses owing to the saccade sequence and other oculomotor covariates. We found that precursor fixations were preceded by the largest saccades among the fixation categories. Independent of the effect of saccade length, EEG amplitude was enhanced in precursor fixations compared with the other fixation categories 200 to 400 ms after fixation onsets, most noticeably over the occipital areas. We concluded that precursor fixations play a pivotal role in visual perception, marking the continuous occurrence of transitions between exploratory and exploitative modes of eye movement in natural viewing behavior.

Neural correlates of task-related refixation behavior.

Eye movement research has shown that attention shifts from the currently fixated location to the next before a saccade is executed. We investigated whether the cost of the attention shift depends on higher-order processing at the time of fixation, in particular on visual working memory load differences between fixations and refixations on task-relevant items. The attention shift is reflected in EEG activity in the saccade-related potential (SRP). In a free viewing task involving visual search and memorization of multiple targets amongst distractors, we compared the SRP in first fixations versus refixations on targets and distractors. The task-relevance of targets implies that more information will be loaded in memory (e.g. both identity and location) than for distractors (e.g. location only). First fixations will involve greater memory load than refixations, since first fixations involve loading of new items, while refixations involve rehearsal of previously visited items. The SRP in the interval preceding the saccade away from a target or distractor revealed that saccade preparation is affected by task-relevance and refixation behavior. For task-relevant items only, we found longer fixation duration and higher SRP amplitudes for first fixations than for refixations over the occipital region and the opposite effect over the frontal region. Our findings provide first neurophysiological evidence that working memory loading of task-relevant information at fixation affects saccade planning.

Refixation patterns reveal memory-encoding strategies in free viewing.

We investigated visual working memory encoding across saccadic eye movements, focusing our analysis on refixation behavior. Over 10-s periods, participants performed a visual search for three, four, or five targets and remembered their orientations for a subsequent change-detection task. In 50% of the trials, one of the targets had its orientation changed. From the visual search period, we scored three types of refixations and applied measures for quantifying eye-fixation recurrence patterns. Repeated fixations on the same regions as well as repeated fixation patterns increased with memory load. Correct change detection was associated with more refixations on targets and less on distractors, with increased frequency of recurrence, and with longer intervals between refixations. The results are in accordance with the view that patterns of eye movement are an integral part of visual working memory representation.

Presaccadic EEG activity predicts visual saliency in free-viewing contour integration.

While viewing a scene, the eyes are attracted to salient stimuli. We set out to identify the brain signals controlling this process. In a contour integration task, in which participants searched for a collinear contour in a field of randomly oriented Gabor elements, a previously established model was applied to calculate a visual saliency value for each fixation location. We studied brain activity related to the modeled saliency values, using coregistered eye tracking and EEG. To disentangle EEG signals reflecting salience in free viewing from overlapping EEG responses to sequential eye movements, we adopted generalized additive mixed modeling (GAMM) to single epochs of saccade-related EEG. We found that, when saliency at the next fixation location was high, amplitude of the presaccadic EEG activity was low. Since presaccadic activity reflects covert attention to the saccade target, our results indicate that larger attentional effort is needed for selecting less salient saccade targets than more salient ones. This effect was prominent in contour-present conditions (half of the trials), but ambiguous in the contour-absent condition. Presaccadic EEG activity may thus be indicative of bottom-up factors in saccade guidance. The results underscore the utility of GAMM for EEG-eye movement coregistration research.

Refixation control in free viewing: a specialized mechanism divulged by eye-movement-related brain activity.

In free viewing, the eyes return to previously visited locations rather frequently, even though the attentional and memory-related processes controlling eye-movement show a strong antirefixation bias. To overcome this bias, a special refixation triggering mechanism may have to be recruited. We probed the neural evidence for such a mechanism by combining eye tracking with EEG recording. A distinctive signal associated with refixation planning was observed in the EEG during the presaccadic interval: the presaccadic potential was reduced in amplitude before a refixation compared with normal fixations. The result offers direct evidence for a special refixation mechanism that operates in the saccade planning stage of eye movement control. Once the eyes have landed on the revisited location, acquisition of visual information proceeds indistinguishably from ordinary fixations. NEW & NOTEWORTHY A substantial proportion of eye fixations in human natural viewing behavior are revisits of recently visited locations, i.e., refixations. Our recently developed methods enabled us to study refixations in a free viewing visual search task, using combined eye movement and EEG recording. We identified in the EEG a distinctive refixation-related signal, signifying a control mechanism specific to refixations as opposed to ordinary eye fixations.

Task modulates functional connectivity networks in free viewing behavior.

In free visual exploration, eye-movement is immediately followed by dynamic reconfiguration of brain functional connectivity. We studied the task-dependency of this process in a combined visual search-change detection experiment. Participants viewed two (nearly) same displays in succession. First time they had to find and remember multiple targets among distractors, so the ongoing task involved memory encoding. Second time they had to determine if a target had changed in orientation, so the ongoing task involved memory retrieval. From multichannel EEG recorded during 200 ms intervals time-locked to fixation onsets, we estimated the functional connectivity using a weighted phase lag index at the frequencies of theta, alpha, and beta bands, and derived global and local measures of the functional connectivity graphs. We found differences between both memory task conditions for several network measures, such as mean path length, radius, diameter, closeness and eccentricity, mainly in the alpha band. Both the local and the global measures indicated that encoding involved a more segregated mode of operation than retrieval. These differences arose immediately after fixation onset and persisted for the entire duration of the lambda complex, an evoked potential commonly associated with early visual perception. We concluded that encoding and retrieval differentially shape network configurations involved in early visual perception, affecting the way the visual input is processed at each fixation. These findings demonstrate that task requirements dynamically control the functional connectivity networks involved in early visual perception.

Combining EEG and eye movement recording in free viewing: Pitfalls and possibilities.

Co-registration of EEG and eye movement has promise for investigating perceptual processes in free viewing conditions, provided certain methodological challenges can be addressed. Most of these arise from the self-paced character of eye movements in free viewing conditions. Successive eye movements occur within short time intervals. Their evoked activity is likely to distort the EEG signal during fixation. Due to the non-uniform distribution of fixation durations, these distortions are systematic, survive across-trials averaging, and can become a source of confounding. We illustrate this problem with effects of sequential eye movements on the evoked potentials and time-frequency components of EEG and propose a solution based on matching of eye movement characteristics between experimental conditions. The proposal leads to a discussion of which eye movement characteristics are to be matched, depending on the EEG activity of interest. We also compare segmentation of EEG into saccade-related epochs relative to saccade and fixation onsets and discuss the problem of baseline selection and its solution. Further recommendations are given for implementing EEG-eye movement co-registration in free viewing conditions. By resolving some of the methodological problems involved, we aim to facilitate the transition from the traditional stimulus-response paradigm to the study of visual perception in more naturalistic conditions.

Fixation duration surpasses pupil size as a measure of memory load in free viewing.

Oculomotor behavior reveals, not only the acquisition of visual information at fixation, but also the accumulation of information in memory across subsequent fixations. Two candidate measures were considered as indicators of such dynamic visual memory load: fixation duration and pupil size. While recording these measures, we displayed an arrangement of 3, 4 or 5 targets among distractors. Both occurred in various orientations. Participants searched for targets and reported whether in a subsequent display one of them had changed orientation. We determined to what extent fixation duration and pupil size indicate dynamic memory load, as a function of the number of targets fixated during the search. We found that fixation duration reflects the number of targets, both when this number is within and above the limit of working memory capacity. Pupil size reflects the number of targets only when it exceeds the capacity limit. Moreover, the duration of fixations on successive targets but not on distractors increases whereas pupil size does not. The increase in fixation duration with number of targets both within and above working memory capacity suggests that in free viewing fixation duration is sensitive to actual memory load as well as to processing load, whereas pupil size is indicative of processing load only. Two alternative models relating visual attention and working memory are considered relevant to these results. We discuss the results as supportive of a model which involves a temporary buffer in the interaction of attention and working memory.