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.

Episodic memory formation in unrestricted viewing.

The brain systems of episodic memory and oculomotor control are tightly linked, suggesting a crucial role of eye movements in memory. But little is known about the neural mechanisms of memory formation across eye movements in unrestricted viewing behavior. Here, we leverage simultaneous eye tracking and EEG recording to examine episodic memory formation in free viewing. Participants memorized multi-element events while their EEG and eye movements were concurrently recorded. Each event comprised elements from three categories (face, object, place), with two exemplars from each category, in different locations on the screen. A subsequent associative memory test assessed participants' memory for the between-category associations that specified each event. We used a deconvolution approach to overcome the problem of overlapping EEG responses to sequential saccades in free viewing. Brain activity was time-locked to the fixation onsets, and we examined EEG power in the theta and alpha frequency bands, the putative oscillatory correlates of episodic encoding mechanisms. Three modulations of fixation-related EEG predicted high subsequent memory performance: (1) theta increase at fixations after between-category gaze transitions, (2) theta and alpha increase at fixations after within-element gaze transitions, (3) alpha decrease at fixations after between-exemplar gaze transitions. Thus, event encoding with unrestricted viewing behavior was characterized by three neural mechanisms, manifested in fixation-locked theta and alpha EEG activity that rapidly turned on and off during the unfolding eye movement sequences. These three distinct neural mechanisms may be the essential building blocks that subserve the buildup of coherent episodic memories during unrestricted viewing behavior.

Perceptual bias contextualized in visually ambiguous stimuli.

The visual appearance of an object is a function of stimulus properties as well as perceptual biases imposed by the observer. The context-specific trade-off between both can be measured accurately in a perceptual judgment task, involving grouping by proximity in ambiguous dot lattices. Such grouping depends lawfully on a stimulus parameter of the dot lattices known as their aspect ratio (AR), whose effect is modulated by a perceptual bias representing the preference for a cardinal orientation. In two experiments, we investigated how preceding context can lead to bias modulation, either in a top-down fashion via visual working memory (VWM) or bottom-up via sensory priming. In Experiment 1, we embedded the perceptual judgment task in a change detection paradigm and studied how the factors of VWM load (complexity of the memory array) and content (congruency in orientation to the ensuing dot lattice) affect the prominence of perceptual bias. A robust vertical orientation bias was observed, which was increased by VWM load and modulated by congruent VWM content. In Experiment 2, dot lattices were preceded by oriented primes. Here, primes regardless of orientation elicited a vertical orientation bias in dot lattices compared to a neutral baseline. Taken together, the two experiments demonstrate that top-down context (VWM load and content) effectively controls orientation bias modulation, while bottom-up context (i.e., priming) merely acts as an undifferentiated trigger to perceptual bias. These findings characterize the temporal context sensitivity of Gestalt perception, shed light on the processes responsible for different perceptual outcomes of ambiguous stimuli, and identify some of the mechanisms controlling perceptual bias.

Effects of Temporal Expectations on the Perception of Motion Gestalts.

Gestalt psychology has traditionally ignored the role of attention in perception, leading to the view that autonomous processes create perceptual configurations that are then attended. More recent research, however, has shown that spatial attention influences a form of Gestalt perception: the coherence of random-dot kinematograms (RDKs). Using ERPs, we investigated whether temporal expectations exert analogous attentional effects on the perception of coherence level in RDKs. Participants were presented fixed-length sequences of RDKs and reported the coherence level of a target RDK. The target was indicated immediately after its appearance by a postcue. Target expectancy increased as the sequence progressed until target presentation; afterward, remaining RDKs were perceived without target expectancy. Expectancy influenced the amplitudes of ERP components P1 and N2. Crucially, expectancy interacted with coherence level at N2, but not at P1. Specifically, P1 amplitudes decreased linearly as a function of RDK coherence irrespective of expectancy, whereas N2 exhibited a quadratic dependence on coherence: larger amplitudes for RDKs with intermediate coherence levels, and only when they were expected. These results suggest that expectancy at early processing stages is an unspecific, general readiness for perception. At later stages, expectancy becomes stimulus specific and nonlinearly related to Gestalt coherence.

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.

Factoring in the spatial effects of symbolic number representation.

Spatial constituents of adult symbolic number representation produce effects of size-value congruity, Spatial Numerical Association of Response Codes (SNARC), and numerical distance. According to behavioral experiments, these effects belong to distinct processing stages. Yet, these effects evoke overlapping responses in both early and late Event Related Potentials (ERPs). To probe whether these overlaps indicate sharing of resources, all relevant stimulus and response conditions were factorially combined in a numerical value comparison task. To secure ERP validity, same numbers were compared against variable reference values. This design resulted in previously unobserved interactions in behavior but inhibited late ERP effects. All effects arose early in the P1 component (around 100 ms) and most showed hemispheric specificity. Independency of congruity and SNARC effects was observed, whereas SNARC and numerical distance were closely intertwined. Differences in hemispheric specificity, rather than stage-wise separation, were key to independence.

High-density scalp EEG data acquired in an inattentional blindness paradigm with background Gestalt stimuli.

Behavioral and electroencephalography (EEG) data were analyzed from 30 participants performing a demanding, attention-capturing task in which they had to detect an occasional decrement of luminance of small discs. Crucially, numerous white segments in the background were presented either in random orientations or configuring a contour shape of a square or a diamond. The participants' awareness of these background configurations was tested with a questionnaire after the first and second sessions. Based on the questionnaire responses, participants were divided into "aware" and "unaware" groups. These data may be of interest to researchers who wish to understand attentional effects on Gestalt integration processes, as well as luminance discrimination.

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.

Target probability modulates fixation-related potentials in visual search.

This study investigated the influence of target probability on the neural response to target detection in free viewing visual search. Participants were asked to indicate the number of targets (one or two) among distractors in a visual search task while EEG and eye movements were co-registered. Target probability was manipulated by varying the set size of the displays between 10, 22, and 30 items. Fixation-related potentials time-locked to first target fixations revealed a pronounced P300 at the centro-parietal cortex with larger amplitudes for set sizes 22 and 30 than for set size 10. With increasing set size, more distractor fixations preceded the detection of the target, resulting in a decreased target probability and, consequently, a larger P300. For distractors, no increase of P300 amplitude with set size was observed. The findings suggest that set size specifically affects target but not distractor processing in overt serial visual search.

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.

Multi-Electrode Alpha tACS During Varying Background Tasks Fails to Modulate Subsequent Alpha Power.

Transcranial alternating-current stimulation (tACS) for entraining alpha activity holds potential for influencing mental function, both in laboratory and clinical settings. While initial results of alpha entrainment are promising, questions remain regarding its translational potential-namely if tACS alpha entrainment is sufficiently robust to context and to what extent it can be upscaled to multi-electrode arrangements needed to direct currents into precise brain loci. We set out to explore these questions by administering alternating current through a multi-electrode montage (mtACS), while varying background task. A multi-electrode analog of previously employed anterior/posterior stimulation failed to replicate the reported alpha entrainment, suggesting that further work is required to understand the scope of applicability of tACS alpha entrainment.

EEG frequency tagging reveals higher order intermodulation components as neural markers of learned holistic shape representations.

Shape perception is intrinsically holistic: combinations of features give rise to configurations with emergent properties that are different from the sum of the parts. The current study investigated neural markers of holistic shape representations learned by means of categorization training. We used the EEG frequency tagging technique, where two parts of a shape stimulus were 'tagged' by modifying their contrast at different temporal frequencies. Signals from both parts are integrated and, as a result, emergent frequency components (so-called, intermodulation responses, IMs), caused by nonlinear interaction of two frequency signals, are observed in the EEG spectrum. First, participants were trained in 4 sessions to discriminate highly similar, unfamiliar shapes into two categories, defined based on the combination of features. After training, EEG was recorded while frequency-tagged shapes from either the trained or the untrained shape family were presented. For all IMs combined, no learning effects were detected, but post hoc analyses of higher-order IMs revealed stronger occipital and occipito-temporal IMs for both trained and untrained exemplars of the trained shape family as compared to the untrained shape family. In line with recent findings, we suggest that the higher-order IMs may reflect high-level visual computations, like holistic shape categorization, resulting from a cascade of non-linear operations. Higher order frequency responses are relatively low in power, hence results should be interpreted cautiously and future research is needed to confirm these effects. In general, these findings are, to our knowledge, the first to show IMs as a neural correlate of perceptual learning.

Large-Scale Traveling Waves in EEG Activity Following Eye Movement.

In spontaneous, stimulus-evoked, and eye-movement evoked EEG, the oscillatory signal shows large scale, dynamically organized patterns of phase. We investigated eye-movement evoked patterns in free-viewing conditions. Participants viewed photographs of natural scenes in anticipation of a memory test. From 200 ms intervals following saccades, we estimated the EEG phase gradient over the entire scalp, and the wave activity, i.e. the goodness of fit of a wave model involving a phase gradient assumed to be smooth over the scalp. In frequencies centered at 6.5 Hz, large-scale phase organization occurred, peaking around 70 ms after fixation onset and taking the form of a traveling wave. According to the wave gradient, most of the times the wave spreads from the posterior-inferior to anterior-superior direction. In these directions, the gradients depended on the size and direction of the saccade. Wave propagation velocity decreased in the course of the fixation, particularly in the interval from 50 to 150 ms after fixation onset. This interval corresponds to the fixation-related lambda activity, which reflects early perceptual processes following fixation onset. We conclude that lambda activity has a prominent traveling wave component. This component consists of a short-term whole-head phase pattern of specific direction and velocity, which may reflect feedforward propagation of visual information at fixation.

Scene Buildup From Latent Memory Representations Across Eye Movements.

An unresolved problem in eye movement research is how a representation is constructed on-line from several consecutive fixations of a scene. Such a scene representation is generally understood to be sparse; yet, for meeting behavioral goals a certain level of detail is needed. We propose that this is achieved through the buildup of latent representations acquired at fixation. Latent representations are retained in an activity-silent manner, require minimal energy expenditure for their maintenance, and thus allow a larger storage capacity than traditional, activation based, visual working memory. The latent representations accumulate and interact in working memory to form to the scene representation. The result is rich in detail while sparse in the sense that it is restricted to the task-relevant aspects of the scene sampled through fixations. Relevant information can quickly and flexibly be retrieved by dynamical attentional prioritization. Latent representations are observable as transient functional connectivity patterns, which emerge due to short-term changes in synaptic weights. We discuss how observing latent representations could benefit from recent methodological developments in EEG-eye movement co-registration.

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.

EEG frequency tagging dissociates between neural processing of motion synchrony and human quality of multiple point-light dancers.

Do we perceive a group of dancers moving in synchrony differently from a group of drones flying in-sync? The brain has dedicated networks for perception of coherent motion and interacting human bodies. However, it is unclear to what extent the underlying neural mechanisms overlap. Here we delineate these mechanisms by independently manipulating the degree of motion synchrony and the humanoid quality of multiple point-light displays (PLDs). Four PLDs moving within a group were changing contrast in cycles of fixed frequencies, which permits the identification of the neural processes that are tagged by these frequencies. In the frequency spectrum of the steady-state EEG we found two emergent frequency components, which signified distinct levels of interactions between PLDs. The first component was associated with motion synchrony, the second with the human quality of the moving items. These findings indicate that visual processing of synchronously moving dancers involves two distinct neural mechanisms: one for the perception of a group of items moving in synchrony and one for the perception of a group of moving items with human quality. We propose that these mechanisms underlie high-level perception of social interactions.

Intermittent regime of brain activity at the early, bias-guided stage of perceptual learning.

Perceptual learning improves visual performance. Among the plausible mechanisms of learning, reduction of perceptual bias has been studied the least. Perceptual bias may compensate for lack of stimulus information, but excessive reliance on bias diminishes visual discriminability. We investigated the time course of bias in a perceptual grouping task and studied the associated cortical dynamics in spontaneous and evoked EEG. Participants reported the perceived orientation of dot groupings in ambiguous dot lattices. Performance improved over a 1-hr period as indicated by the proportion of trials in which participants preferred dot groupings favored by dot proximity. The proximity-based responses were compromised by perceptual bias: Vertical groupings were sometimes preferred to horizontal ones, independent of dot proximity. In the evoked EEG activity, greater amplitude of the N1 component for horizontal than vertical responses indicated that the bias was most prominent in conditions of reduced visual discriminability. The prominence of bias decreased in the course of the experiment. Although the bias was still prominent, prestimulus activity was characterized by an intermittent regime of alternating modes of low and high alpha power. Responses were more biased in the former mode, indicating that perceptual bias was deployed actively to compensate for stimulus uncertainty. Thus, early stages of perceptual learning were characterized by episodes of greater reliance on prior visual preferences, alternating with episodes of receptivity to stimulus information. In the course of learning, the former episodes disappeared, and biases reappeared only infrequently.

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.