Dealing with artifacts: The EOG contamination of the event-related brain potential

Eye movements and blinks represent a major source of artifacts in the electroencephalogram (EEG) and event-related brain potentials (ERPs). The origin of this artifact is the large difference in potential that exists between the cornea and the retina. Eye movements and blinks produce shifts of the electric fields that propagate across the whole head and that can be several times larger than the activity generated by the brain. Ocular activity can be monitored by electrodes located near the eyes (electrooculogram, or EOG). The electric fields associated with eye movements and blinks are somewhat different. The simplest procedure for dealing with ocular artifacts is to eliminate trials on which EOG activity is detected (rejection). However, this technique may result in data loss and biased data samples, especially when one is comparing clinical populations or tasks involving large amounts of eye movements. Another approach involves estimation and correction of the ocular artifact on the EEG and ERP traces. Several techniques have been proposed. Some of them are reviewed in the present paper. Issues related to the accuracy of the various techniques, as well as other advantages and limitations, are also discussed. Finally, general guidelines for how to deal with ocular artifacts are proposed.     

Field independence, lateralization and defensive style

This study investigated the relationship between field independence and defense clustering as measured by the Defense Mechanisms Inventory and lateral eye movements. Subjects had previously been classified either as hysterical or obsessive style by the Rorschach and WAIS Comprehension subtest. Previous findings indicate that these subjects have a preferred direction of lateral eye movement in a questioning format (hysterical style = left; obsessive style = right). This study found no relationship between field independence and defense clustering and lateral eye movements. To the extent that eye gaze indexes hemispheric activation, we conclude that neither field independence nor defense clustering was related to hemispheric lateralization.     

Pharmacological treatment effects on eye movement control

The increasing use of eye movement paradigms to assess the functional integrity of brain systems involved in sensorimotor and cognitive processing in clinical disorders requires greater attention to effects of pharmacological treatments on these systems. This is needed to better differentiate disease and medication effects in clinical samples, to learn about neurochemical systems relevant for identified disturbances, and to facilitate identification of oculomotor biomarkers of pharmacological effects. In this review, studies of pharmacologic treatment effects on eye movements in healthy individuals are summarized and the sensitivity of eye movements to a variety of pharmacological manipulations is established. Primary findings from these studies of healthy individuals involving mainly acute effects indicate that: (i) the most consistent finding across several classes of drugs, including benzodiazepines, first- and second- generation antipsychotics, anticholinergic agents, and anticonvulsant/mood stabilizing medications is a decrease in saccade and smooth pursuit velocity (or increase in saccades during pursuit); (ii) these oculomotor effects largely reflect the general sedating effects of these medications on central nervous system functioning and are often dose-dependent; (iii) in many cases changes in oculomotor functioning are more sensitive indicators of pharmacological effects than other measures; and (iv) other agents, including the antidepressant class of serotonergic reuptake inhibitors, direct serotonergic agonists, and stimulants including amphetamine and nicotine, do not appear to adversely impact oculomotor functions in healthy individuals and may well enhance aspects of saccade and pursuit performance. Pharmacological treatment effects on eye movements across several clinical disorders including schizophrenia, affective disorders, attention deficit hyperactivity disorder, Parkinson’s disease, and Huntington’s disease are also reviewed. While greater recognition and investigation into pharmacological treatment effects in these disorders is needed, both beneficial and adverse drug effects are identified. This raises the important caveat for oculomotor studies of neuropsychiatric disorders that performance differences from healthy individuals cannot be attributed to illness effects alone. In final sections of this review, studies are presented that illustrate the utility of eye movements for use as potential biomarkers in pharmacodynamic and pharmacogenetic studies. While more systematic studies are needed, we conclude that eye movement measurements hold significant promise as tools to investigate treatment effects on cognitive and sensorimotor processes in clinical populations and that their use may be helpful in speeding the drug development pathway for drugs targeting specific neural systems and in individualizing pharmacological treatments.     

Pharmacological treatment effects on eye movement control

The increasing use of eye movement paradigms to assess the functional integrity of brain systems involved in sensorimotor and cognitive processing in clinical disorders requires greater attention to effects of pharmacological treatments on these systems. This is needed to better differentiate disease and medication effects in clinical samples, to learn about neurochemical systems relevant for identified disturbances, and to facilitate identification of oculomotor biomarkers of pharmacological effects. In this review, studies of pharmacologic treatment effects on eye movements in healthy individuals are summarized and the sensitivity of eye movements to a variety of pharmacological manipulations is established. Primary findings from these studies of healthy individuals involving mainly acute effects indicate that: (i) the most consistent finding across several classes of drugs, including benzodiazepines, first- and second- generation antipsychotics, anticholinergic agents, and anticonvulsant/mood stabilizing medications is a decrease in saccade and smooth pursuit velocity (or increase in saccades during pursuit); (ii) these oculomotor effects largely reflect the general sedating effects of these medications on central nervous system functioning and are often dose-dependent; (iii) in many cases changes in oculomotor functioning are more sensitive indicators of pharmacological effects than other measures; and (iv) other agents, including the antidepressant class of serotonergic reuptake inhibitors, direct serotonergic agonists, and stimulants including amphetamine and nicotine, do not appear to adversely impact oculomotor functions in healthy individuals and may well enhance aspects of saccade and pursuit performance. Pharmacological treatment effects on eye movements across several clinical disorders including schizophrenia, affective disorders, attention deficit hyperactivity disorder, Parkinson’s disease, and Huntington’s disease are also reviewed. While greater recognition and investigation into pharmacological treatment effects in these disorders is needed, both beneficial and adverse drug effects are identified. This raises the important caveat for oculomotor studies of neuropsychiatric disorders that performance differences from healthy individuals cannot be attributed to illness effects alone. In final sections of this review, studies are presented that illustrate the utility of eye movements for use as potential biomarkers in pharmacodynamic and pharmacogenetic studies. While more systematic studies are needed, we conclude that eye movement measurements hold significant promise as tools to investigate treatment effects on cognitive and sensorimotor processes in clinical populations and that their use may be helpful in speeding the drug development pathway for drugs targeting specific neural systems and in individualizing pharmacological treatments.     

Attention and saccadic eye movements

Four threshold detection experiments addressed three issues concerning the relationship between movements of spatial attention and saccadic eye movements: (a) the time course of attention shifts wit saccades, (b) the response of the two systems to changes in stimulus parameters, and (c) the relationship of attention to saccadic suppression. These issues bear on the more general question of the degree of independence between the saccadic and attentional movement systems. The results of these experiments support the contention that the mechanisms that shift attention are separate from those that control saccadic eye movements. Relevant events in the visual field periphery, however, will trigger both a saccade and attention shift. The attentional response to such events does not appear to be under subjects' control. The implication of these results for theories of saccadic suppression is discussed.     

Effects of handedness and saccadic bilateral eye movements on components of autobiographical recollection

The effects of handedness and saccadic bilateral eye movements on autobiographical recollection were investigated. Recall of autobiographical memories was cued by the use of neutral and emotional words. Autobiographical recollection was assessed by the autobiographical memory questionnaire. Experiment 1 found that mixed-handed (vs. right handed) individuals demonstrated greater levels of autobiographical recollection on the components of seeing, hearing, and emotion. Experiment 2 found that following 30 s of bilateral eye movements, greater levels of autobiographical recollection were demonstrated on the components of reliving, seeing, hearing, emotion, self-perspective and veridicality. The results extend previous research by showing that the recollective components of real world memories can be enhanced by either mixed-handedness or eye movements. In addition, these results provide a bridge between laboratory studies of recollection and autobiographical recollection. The findings are considered in terms of research on the cognitive neuroscience of autobiographical memory.     

Development of eye-movement control

Cognitive control of behavior continues to improve through adolescence in parallel with important brain maturational processes including synaptic pruning and myelination, which allow for efficient neuronal computations and the functional integration of widely distributed circuitries supporting top-down control of behavior. This is also a time when psychiatric disorders, such as schizophrenia and mood disorders, emerge reflecting a particularly vulnerability to impairments in development during adolescence. Oculomotor studies provide a unique neuroscientific approach to make precise associations between cognitive control and brain circuitry during development that can inform us of impaired systems in psychopathology. In this review, we first describe the development of pursuit, fixation, and visually-guided saccadic eye movements, which collectively indicate early maturation of basic sensorimotor processes supporting reflexive, exogenously-driven eye movements. We then describe the literature on the development of the cognitive control of eye movements as reflected in the ability to inhibit a prepotent eye movement in the antisaccade task, as well as making an eye movement guided by on-line spatial information in working memory in the oculomotor delayed response task. Results indicate that the ability to make eye movements in a voluntary fashion driven by endogenous plans shows a protracted development into adolescence. Characterizing the transition through adolescence to adult-level cognitive control of behavior can inform models aimed at understanding the neurodevelopmental basis of psychiatric disorders.     

Inverting faces does not abolish cultural diversity in eye movements

Face processing is widely understood to be a basic, universal visual function effortlessly achieved by people from all cultures and races. The remarkable recognition performance for faces is markedly and specifically affected by picture-plane inversion: the so-called face-inversion effect (FIE), a finding often used as evidence for face-specific mechanisms. However, it has recently been shown that culture shapes the way people deploy eye movements to extract information from faces. Interestingly, the comparable lack of experience with inverted faces across cultures offers a unique opportunity to establish the extent to which such cultural perceptual biases in eye movements are robust, but also to assess whether face-specific mechanisms are universally tuned. Here we monitored the eye movements of Western Caucasian (WC) and East Asian (EA) observers while they learned and recognised WC and EA inverted faces. Both groups of observers showed a comparable impairment in recognising inverted faces of both races. WC observers deployed a scattered inverted triangular scanpath with a bias towards the mouth, whereas EA observers uniformly extended the focus of their fixations from the centre towards the eyes. Overall, our data show that cultural perceptual differences in eye movements persist during the FIE, questioning the universality of face-processing mechanisms.     

眼睛运动如何与记忆相关？

很久以来,人们一直在致力于研究人的眼动与心理活动之间的关系,从而揭示其间的奥妙。众多研究表明,睡眠时的快速眼动（RapidEyeMovements,REM）及其周期对记忆的形成与巩固有重要作用。在清醒状态下,人的眼动就是为了获得视觉信息,如果涉及记忆任务,这就是编码阶段的具体行动。另外,问题解决过程也有眼动参与。总体看来,眼动和记忆之间是一种双向的关系,适当的眼动训练或许能够提高记忆成绩。     

Neurophysiology and neuroanatomy of smooth pursuit in humans

Smooth pursuit eye movements enable us to focus our eyes on moving objects by utilizing well-established mechanisms of visual motion processing, sensorimotor transformation and cognition. Novel smooth pursuit tasks and quantitative measurement techniques can help unravel the different smooth pursuit components and complex neural systems involved in its control. The maintenance of smooth pursuit is driven by a combination of the prediction of target velocity and visual feedback about performance quality, thus a combination of retinal and extraretinal information that has to be integrated in various networks. Different models of smooth pursuit with specific in- and output parameters have been developed for a better understanding of the underlying neurophysiological mechanisms and to make quantitative predictions that can be tested in experiments. Functional brain imaging and neurophysiological studies have defined motion sensitive visual area V5, frontal (FEF) and supplementary (SEF) eye fields as core cortical smooth pursuit regions. In addition, a dense neural network is involved in the adjustment of an optimal smooth pursuit response by integrating also extraretinal information. These networks facilitate interaction of the smooth pursuit system with multiple other visual and non-visual sensorimotor systems on the cortical and subcortical level. Future studies with fMRI advanced techniques (e.g., event-related fMRI) promise to provide an insight into how smooth pursuit eye movements are linked to specific brain activation. Applying this approach to neurological and also mental illness can reveal distinct disturbances within neural networks being present in these disorders and also the impact of medication on this circuitry.     

Neurophysiology and neuroanatomy of smooth pursuit in humans

Smooth pursuit eye movements enable us to focus our eyes on moving objects by utilizing well-established mechanisms of visual motion processing, sensorimotor transformation and cognition. Novel smooth pursuit tasks and quantitative measurement techniques can help unravel the different smooth pursuit components and complex neural systems involved in its control. The maintenance of smooth pursuit is driven by a combination of the prediction of target velocity and visual feedback about performance quality, thus a combination of retinal and extraretinal information that has to be integrated in various networks. Different models of smooth pursuit with specific in- and output parameters have been developed for a better understanding of the underlying neurophysiological mechanisms and to make quantitative predictions that can be tested in experiments. Functional brain imaging and neurophysiological studies have defined motion sensitive visual area V5, frontal (FEF) and supplementary (SEF) eye fields as core cortical smooth pursuit regions. In addition, a dense neural network is involved in the adjustment of an optimal smooth pursuit response by integrating also extraretinal information. These networks facilitate interaction of the smooth pursuit system with multiple other visual and non-visual sensorimotor systems on the cortical and subcortical level. Future studies with fMRI advanced techniques (e.g., event-related fMRI) promise to provide an insight into how smooth pursuit eye movements are linked to specific brain activation. Applying this approach to neurological and also mental illness can reveal distinct disturbances within neural networks being present in these disorders and also the impact of medication on this circuitry.     

Removing the own-race bias in face recognition by attentional shift using fixation crosses to diagnostic features: An eye-tracking study

Hills and Lewis (2011) have demonstrated that the own-race bias in face recognition can be reduced or even removed by guiding participants' attention and potentially eye movements to the most diagnostic visual features. Using the same old/new recognition paradigm as Hills and Lewis, we recorded Black and White participants' eye movements whilst viewing Black and White faces following fixation crosses that preceded the bridge of the nose (between the eyes) or the tip of the nose. White faces were more accurately recognized when following high fixation crosses (that preceded the bridge of the nose) than when following low fixation crosses. The converse was true for Black faces. These effects were independent of participant race. The fixation crosses attracted the first fixation but had less effect on other eye-tracking measures. Furthermore, the location of the first fixation was predictive of recognition accuracy. These results are consistent with an attentional allocation model of the own-race bias in face recognition and highlight the importance of the first fixation for face perception (cf. Hsiao & Cottrell, 2008).     

Looking to understand: the coupling between speakers' and listeners' eye movements and its relationship to discourse comprehension

We investigated the coupling between a speaker's and a listener's eye movements. Some participants talked extemporaneously about a television show whose cast members they were viewing on a screen in front of them. Later, other participants listened to these monologues while viewing the same screen. Eye movements were recorded for all speakers and listeners. According to cross-recurrence analysis, a listener's eye movements most closely matched a speaker's eye movements at a delay of 2 sec. Indeed, the more closely a listener's eye movements were coupled with a speaker's, the better the listener did on a comprehension test. In a second experiment, low-level visual cues were used to manipulate the listeners' eye movements, and these, in turn, influenced their latencies to comprehension questions. Just as eye movements reflect the mental state of an individual, the coupling between a speaker's and a listener's eye movements reflects the success of their communication.     

自然阅读的脑成像研究及其与眼动技术结合

以往的研究者主要采用单词系列呈现的实验范式对词、句子和篇章等材料进行阅读脑成像研究。针对近年来使用自然阅读范式的功能磁共振(fMRI)研究进行分析,建议在该范式下使用脑-眼动同步记录的方式,并介绍了基于注视编码的fMRI数据分析原理。新的范式和技术提高了fMRI研究的生态效度,有利于对阅读中眼动加工的脑机制进行探索,是相关研究的新趋势。未来需要在自然阅读fMRI实验中结合实验设计及其他技术以克服时间分辨率低的问题,同时要注意探讨阅读和眼动脑区的关系。     

语言认知中眼动和ERP结合的理论、技术路径及其应用

自然语言的产生和理解具有高度的实时性。眼动和ERP技术具有很高的时间分辨率, 可以在线测查语言认知加工过程。然而, 两种技术手段都各有利弊, 可以在一定程度上进行互补, 从而为揭示语言加工的特点和机制提供行为和电生理证据。在文献梳理的基础上, 详细分析了语言认知中眼动和ERP技术结合的必要性, 即注视和加工的耦合程度以及眼睛和大脑的加工速度; 准确阐述了眼动和ERP结合的技术路径, 即眼动和ERP单独记录、ERP结合眼电分析、眼动和ERP同步记录, 比较了不同方法的优缺点; 具体介绍了眼动和ERP结合在语言认知研究中的应用。最后, 对眼动和ERP结合在未来研究中需解决的问题进行了展望。     

Knowledge organization and skill differences in computer programmers

Like experts in other fields, expert computer programmers can recall at a glance far more information relevant to their field than novices can. One explanation for this difference is that experts not only have more information, they have it better organized into meaningful chunks. In this paper, we infer the details of individual programmers' chunks of key programming concepts using the Reitman—Rueter (Cognitive Psychology, 1980, 12(4), 554–581.) technique for inferring tree structures from recall orders. Differences in organizations accompany skill-level differences. Beginner programmers' organizations show a rich variety of common-language associations to these programming concepts; Intermediate programmers show mixtures of programming and common-language associations; and Experts show remarkably similar, but not identical, organizations based clearly on programming knowledge.     

The relationship between eye movements and spatial attention

Most previous studies of the attentional consequences of making saccadic eye movements have used peripheral stimuli to elicit eye movements. It is argued that in the light of evidence showing automatic “capture” of attention by peripheral stimuli, these experiments do not distinguish between attentional effects due to peripheral stimuli and those due to eye movements. In the present study, spatial attention was manipulated by varying the probability that peripheral probe stimuli would appear in different positions, while saccades were directed by a central arrow, enabling the effects of attention and eye movements to be separated. The results showed that the time to react to a peripheral stimulus could be shortened both by advance knowledge of its likely position and, separately, by preparing to make a saccade to that position. When the saccade was directed away from the most likely position of the probe, the targets for attention and eye movements were on opposite sides of the display. In this condition, the effects of preparing to make a saccade proved to be stronger than the effects of attentional allocation until well after the saccade had finished, suggesting that making a saccade necessarily involves the allocation of attention to the target position. The effects of probe stimuli on saccade latencies were also examined: probe stimuli that appeared before the saccade shortened saccade latencies if they appeared at the saccade target, and lengthened saccade latencies if they appeared on the opposite side of fixation. These facilitatory and inhibitory effects were shown to occur at different stages of saccade preparation and suggest that attention plays an important role in the generation of voluntary eye movements. The results of this study indicate that while it is possible to make attention movements without making corresponding eye movements, it is not possible to make an eye movement (in the absence of peripheral stimulation) without making a corresponding shift in the focus of attention.     

汉字笔画数对注视位置效应的影响

采用EyeLink 2000眼动仪,选取四种不同类型的双字词（首字和尾字均为多笔画汉字;首字为多笔画汉字,尾字为少笔画汉字;首字为少笔画汉字,尾字为多笔画汉字;首字和尾字均为少笔画汉字）,要求被试阅读包含有目标词的句子,以探讨汉字笔画数对注视位置效应的影响。结果发现,单次注视条件下,读者往往将首次注视定位于词的中心位置,多次注视时首次注视往往落在词的开头部分;但是当首字为多笔画汉字时,相较于首字为少笔画汉字,读者对目标词的首次注视更多地落在词的首字上。首字和尾字笔画数共同影响读者对目标词的再注视概率。研究结果支持“战略-战术”模型。     

Detecting eye movements in dynamic environments

To take advantage of the increasing number of in-vehicle devices, automobile drivers must divide their attention between primary (driving) and secondary (operating in-vehicle device) tasks. In dynamic environments such as driving, however, it is not easy to identify and quantify how a driver focuses on the various tasks he/she is simultaneously engaged in, including the distracting tasks. Measures derived from the driver’s scan path have been used as correlates of driver attention. This article presents a methodology for analyzing eye positions, which are discrete samples of a subject’s scan path, in order to categorize driver eye movements. Previous methods of analyzing eye positions recorded in a dynamic environment have relied completely on the manual identification of the focus of visual attention from a point of regard superimposed on a video of a recorded scene, failing to utilize information regarding movement structure in the raw recorded eye positions. Although effective, these methods are too time consuming to be easily used when the large data sets that would be required to identify subtle differences between drivers, under different road conditions, and with different levels of distraction are processed. The aim of the methods presented in this article are to extend the degree of automation in the processing of eye movement data by proposing a methodology for eye movement analysis that extends automated fixation identification to include smooth and saccadic movements. By identifying eye movements in the recorded eye positions, a method of reducing the analysis of scene video to a finite search space is presented. The implementation of a software tool for the eye movement analysis is described, including an example from an on-road test-driving sample.     

The effects of eye and limb movements on working memory

Three experiments examined the role of eye and limb movements in the maintenance of information in spatial working memory. In Experiment 1, reflexive saccades interfered with memory span for spatial locations but did not interfere with memory span for letters. In Experiment 2, three different types of eye movements (reflexive saccades, pro-saccades, and anti-saccades) interfered with working memory to the same extent. In all three cases, spatial working memory was much more affected than verbal working memory. The results of these two experiments suggest that eye movements interfere with spatial working memory primarily by disrupting processes localised in the visuospatial sketchpad. In Experiment 3, limb movements performed while maintaining fixation produced as much interference with spatial working memory as reflexive saccades. These results suggest that the interference produced by eye movements is not the result of their visual consequences. Rather, all spatially directed movements appear to have similar effects on visuospatial working memory.