Cognitive control of saccadic eye movements

The saccadic eye movement system provides researchers with a powerful tool with which to explore the cognitive control of behaviour. It is a behavioural system whose limited output can be measured with exceptional precision, and whose input can be controlled and manipulated in subtle ways. A range of cognitive processes (notably those involved in working memory and attention) have been shown to influence saccade parameters. Researchers interested in the relationship between cognitive function and psychiatric disorders have made extensive use of saccadic eye movement tasks to draw inferences as to the cognitive deficits associated with particular psychopathologies. The purpose of this review is to provide researchers with an overview of the research literature documenting cognitive involvement in saccadic tasks in healthy controls. An appreciation of this literature provides a solid background against which to interpret the deficits on saccadic tasks demonstrated in patient populations.     

Neurophysiology and neuroanatomy of reflexive and voluntary saccades in non-human primates

A multitude of cognitive functions can easily be tested by a number of relatively simple saccadic eye movement tasks. This approach has been employed extensively with patient populations to investigate the functional deficits associated with psychiatric disorders. Neurophysiological studies in non-human primates performing the same tasks have begun to provide us with insights into the neural mechanisms underlying many cognitive functions. Here, we review studies that have investigated single neuron activity in the superior colliculus (see glossary), frontal eye field, supplementary eye field, dorsolateral prefrontal cortex, anterior cingulate (see glossary) cortex and lateral intraparietal area associated with the performance of visually guided saccades, anti-saccades and memory-guided saccades in awake behaving monkeys.     

Neurophysiology and neuroanatomy of reflexive and voluntary saccades in non-human primates

A multitude of cognitive functions can easily be tested by a number of relatively simple saccadic eye movement tasks. This approach has been employed extensively with patient populations to investigate the functional deficits associated with psychiatric disorders. Neurophysiological studies in non-human primates performing the same tasks have begun to provide us with insights into the neural mechanisms underlying many cognitive functions. Here, we review studies that have investigated single neuron activity in the superior colliculus (see glossary), frontal eye field, supplementary eye field, dorsolateral prefrontal cortex, anterior cingulate (see glossary) cortex and lateral intraparietal area associated with the performance of visually guided saccades, anti-saccades and memory-guided saccades in awake behaving monkeys.     

Detecting drivers’ cognitive load from saccadic intrusion

In this paper, we have explored use of Saccadic Intrusion to detect drivers’ cognitive load and instantaneous perception of developing road hazards. Saccadic Intrusion is a type of eye gaze movement which was earlier found to be related to change in cognitive load. We have developed an algorithm to detect saccadic intrusion from a commercially available low-cost eye gaze tracker and conducted four user studies involving a driving simulator and cognitive and hazard perception tests. Our results show that average velocities of saccadic intrusion increases with increase in cognitive load and recording saccadic intrusion and eye blinks for 6 s duration can predict drivers’ instantaneous perception of developing road hazards.     

眼跳的研究范式及其主要认知功能

眼跳运动系统为研究者探索行为的认知控制机制提供了有力工具。已有研究发现,很多认知过程会影响不同类型眼跳任务中的眼跳参数。在系统梳理已有研究的基础上,从以下4个方面系统阐述和评价了眼跳运动的研究范式和主要认知功能：（1）视觉导向眼跳的研究范式和变式及其认知功能,包括空白/重叠效应、分心物效应、提示效应、学习效应等;（2）预测性眼跳的研究范式和认知控制,涉及神经生物钟理论、视空间工作记忆、指导语等;（3）记忆导向眼跳的研究范式和变式及其认知控制,包括分心物效应、年龄效应、视空间工作记忆的抑制效应、注意等;（4）反向眼跳的研究范式和变式及其认知控制,包括反向眼跳抑制、眼跳决策信号竞争整合模型、工作记忆容量、注意、错误监控、学习、奖励和年龄效应等。最后,结合已有研究范式对未来眼跳研究的趋势和需解决的问题进行了展望。     

Looking for answers: eye movements in non-visual cognitive tasks

It is not known why people move their eyes when engaged in non-visual cognition. The current study tested the hypothesis that differences in saccadic eye movement rate (EMR) during non-visual cognitive tasks reflect different requirements for searching long-term memory. Participants performed non-visual tasks requiring relatively low or high long-term memory retrieval while eye movements were recorded. In three experiments, EMR was substantially lower for low-retrieval than for high-retrieval tasks, including in an eyes closed condition in Experiment 3. Neither visual imagery nor between-task difficulty was related to EMR, although there was some evidence for a minor effect of within-task difficulty. Comparison of task-related EMRs to EMR during a no-task waiting period suggests that eye movements may be suppressed or activated depending on task requirements. We discuss a number of possible interpretations of saccadic eye movements during non-visual cognition and propose an evolutionary model that links these eye movements to memory search through an elaboration of circuitry involved in visual perception.     

Interdependence of Saccadic and Fixational Fluctuations

Recent research suggests that the different components of eye movements (fixations, saccades) are not strictly separate but are interdependent processes. This argument rests on observations that gaze-step sizes yield unimodal distributions and exhibit power-law scaling, indicative of interdependent processes coordinated across timescales. The studies that produced these findings, however, employed complex tasks (visual search, scene perception). Thus, the question is whether the observed interdependence is a fundamental property of eye movements or emerges in the interplay between cognitive processes and complex visual stimuli. In this study, we used a simple eye movement task where participants moved their eyes in a prescribed sequence at several different paces. We outlined diverging predictions for this task for independence versus interdependence of fixational and saccadic fluctuations and tested these predictions by assessing the spectral properties of eye movements. We found no clear peak in the power spectrum attributable exclusively to saccadic fluctuations. Furthermore, changing the pace of the eye movement sequence yielded a global shift in scaling relations evident in the power spectrum, not just a localized shift for saccadic fluctuations. These results support the conclusion that fixations and saccades are interdependent processes.     

Saccadic eye movements: what do they tell us about aging cognition?

Although the relationship between age-related cognitive decline and saccadic eye movement (SEM) deficits has been outlined, specific cognitive alterations underlying age-related changes in saccadic performance remain unclear. This study attempted to better understand the nature of aging effects on SEMs. We compared SEMs in younger and older adults in prosaccade (PS) and antisaccade (AS) tasks under gap, step, and overlap conditions. We also examined relationships between these performances and several neuropsychological scores. Twenty-eight younger adults (YA), 24 older adults under 65 years (OA_<65) and 24 over 65 years (OA_>65) of age completed a neuropsychological evaluation, PS and AS tasks. Our results showed that latencies, AS cost, time to correct AS errors, and uncorrected AS, increased with aging. YA showed higher overlap effects than OA_>65 and OA_<65. Importantly, correlations and regressions revealed close relationships not only between latencies and processing speed measures but also between the AS cost and the inhibition process measures. Correct saccades and the time to correct AS errors were closely related to the inhibition process and cognitive flexibility measures. These findings suggest that the progressive age-related decline of processing speed and executive attention are associated with, and can be highlighted though SEMs in PS and AS tasks.     

Oculomotor atypicalities in Developmental Coordination Disorder

Children with Developmental Coordination Disorder (DCD) fail to acquire adequate motor skill, yet surprisingly little is known about the oculomotor system in DCD. Successful completion of motor tasks is supported by accurate visual feedback. The purpose of this study was to determine whether any oculomotor differences can distinguish between children with and without a motor impairment. Using eye tracking technology, visual fixation, smooth pursuit, and pro‐ and anti‐saccade performance were assessed in 77 children that formed three groups: children with DCD (aged 7–10), chronologically age (CA) matched peers, and a motor‐match (MM) group (aged 4–7). Pursuit gain and response preparation in the pro‐ and anti‐saccade tasks were comparable across groups. Compared to age controls, children with DCD had deficits in maintaining engagement in the fixation and pursuit tasks, and made more anti‐saccade errors. The two typically developing groups performed similarly, except on the fast speed smooth pursuit and antisaccade tasks, where the CA group outperformed the younger MM group. The findings suggest that children with DCD have problems with saccadic inhibition and maintaining attention on a visual target. Developmental patterns were evident in the typically developing groups, suggesting that the pursuit system and cognitive control develop with age. This study adds to the literature by being the first to systematically identify specific oculomotor differences between children with and without a motor impairment. Further examination of oculomotor control may help to identify underlying processes contributing to DCD. A video abstract of this article can be viewed at: https://youtu.be/NinXa2KlB4M . [Correction added on 27 January 2017, after first online publication: The video abstract link was added.]     

气质与眼动控制的关系

本研究采用眼动追踪和问卷测量相结合的方法,对气质类型和眼动控制的关系进行了探讨。眼动实验为2（眼跳方向：朝向眼跳和反向眼跳）X 2（任务类型：重复眼跳和转换眼跳）组内设计;气质分数用陈会昌编制的《气质类型测试量表》测量。结果表明,气质分数与眼动特性之间存在显著的相关性,不同气质类型（神经活动类型）在抑制过程和任务重置过程中表现出不同的相互作用模式。具体而言,神经活动强度是一个基本维度,它与认知控制的抑制功能和转换功能都有着密切联系;而神经活动的灵活性和平衡性则分别是转换功能和抑制功能的重要条件。     

Why do we move our eyes while trying to remember? The relationship between non-visual gaze patterns and memory

Non-visual gaze patterns (NVGPs) involve saccades and fixations that spontaneously occur in cognitive activities that are not ostensibly visual. While reasons for their appearance remain obscure, convergent empirical evidence suggests that NVGPs change according to processing requirements of tasks. We examined NVPGs in tasks with long-term memory (LTM) and working memory (WM) requirements. Experiment 1 yielded significantly higher eye movement rate (EMR) in tasks requiring LTM search than in a WM task requiring maintenance of information. Experiment 2 manipulated accessibility of items in study-test episodic tasks using the levels of processing paradigm. EMR was high in episodic recall irrespective of item accessibility. Experiment 3 examined functional significance of saccades in LTM tasks. Voluntary saccadic suppression produced no evidence that saccades contribute to task performance. We discuss the apparent epiphenomenal nature of spontaneous saccades from an evolutionary perspective and outline a neuroanatomical model of the link between the saccadic and memory system.     

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.     

Remembering a location makes the eyes curve away

Working memory is a system that keeps limited information on-line for immediate access by cognitive processes. This type of active maintenance is important for everyday life activities. The present study shows that maintaining a location in spatial working memory affects the trajectories of saccadic eye movements toward visual targets, as the eyes deviate away from the remembered location. This finding provides direct evidence for a strong overlap between spatial working memory and the eye movement system. We argue that curvature is the result of the need to inhibit memory-based eye movement activity in the superior colliculus, in order to allow an accurate saccade to the visual target. Whereas previous research has shown that the eyes may deviate away from visually presented stimuli that need to be ignored, we show that the eyes also curve away from remembered stimuli.     

Interference effects between saccadic and key-press reaction times of volleyball players and nonathletes

To investigate the interference effect in volleyball players and nonathletes (ns=10) when they executed both saccadic and key-press reaction time (RT) tasks concurrently, the two groups responded to the onset of peripheral visual stimuli as quickly as possible in single and dual conditions. In the single condition, subjects responded with either saccadic eye or key-press movement. In the dual condition, they responded concurrently with both saccadic eye and key-press movements. In both groups, the key-press RT was longer in the dual condition than in the single condition. However, the amount of key-press RT delay was remarkably smaller for the volleyball players than for nonathletes. This suggests the motor command to initiate manual movement of volleyball players might be less interfered with by a concurrent oculomotor command to initiate saccadic eye movement when compared to that of nonathletes.     

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 tell-tale tasks: a review of saccadic research in psychiatric patient populations

This review focuses on saccade research with adult psychiatric patients. It begins with an introduction of the various types of saccades and the tasks used to evoke them. The functional significance of the different types of eye movements is briefly discussed. Research findings regarding the saccadic performance of different adult psychiatric patient populations are discussed in detail, with particular emphasis on findings regarding error rates, response latencies, and any specific task parameters that might affect those variables. Findings regarding the symptom, neurocognitive, and neural correlates of saccadic performance and the functional significance of patients’ saccadic deficits are also discussed. We also discuss the saccadic deficits displayed by various patient groups in terms of circuitry (e.g. cortical/basal ganglia circuits) that may be implicated in the underlying pathophysiology of several of these disorders. Future directions for research in this growing area are offered.     

婴儿心理理论的发展:表现和机制

婴儿心理理论发展研究是探索人类社会认知起源、发生和发展的重要领域.从联合注意、情绪理解、意图理解、愿望理解和错误信念理解等方面分析了几个月至3岁左右的婴儿心理理论发生和发展的研究现状.为了探讨3岁以下婴儿心理理论的发展过程,研究者发展了一些适合婴儿语言和行为发展特征的非言语和言语测试任务,包括非言语自发—反应错误信念任务、言语自发—反应错误信念任务,同时也采用眼动技术和事件相关电位技术来考察心理理论发展水平和发展机制.婴儿心理理论的发生和发展在不同测试任务上表现出一定的年龄特征.这与认知功能(如语言、执行功能)的发展、环境因素(如家庭、同伴、文化)以及神经系统发育有关.也有一些最新研究从心理理论发生和发展的基因、激素水平进行了探讨.最后提出了该领域未来研究可以进一步探讨的问题.     

Representation and learning in motor action – Bridges between experimental research and cognitive robotics

To gain a better understanding of the functionality of representation and categorization in action and interaction, it is fundamental that researchers understand how movements are represented in long-term memory. It is our position that human motor control requires that our actions be planned and represented in terms of intended perceptual effects and future task demands, and that the individual has a well-structured mental representation of the task so that the movement can be carried out successfully. Basic Action Concepts (BACs) are identified as major building blocks of cognitive representation in long-term memory, which are cognitive tools used to master the functional demands of movement tasks. In this paper, we consider relevant issues in research methodology and present an experimental method that can be used to assess action-relevant representational structures. This method permits us to observe the strong relationship between cognitive representation and performance in manual action. For example, the specific differences in the mental representations of participants are strongly related to skill level, as well as biomechanical and task constraints. We then discuss results from our learning experiments, where we have examined the development and changes in cognitive representation over time. From these experiments we have found that cognitive reference structures include task-specific spatial information, which provides the basis for action control in skilled voluntary movement. We have implemented these results on various robotic platforms. We argue that the insights gained from various experimental approaches in the field of cognitive psychology and motor control enable researchers to explore the possibilities and limitations of artificial control architectures in robot systems. Finally, we argue that this is not a unidirectional process. Researchers from the field of cognitive psychology and motor control can profit from the advances in technological systems, which enhance the understanding of human motor control in skilled voluntary action.     

Saccades predict and synchronize to visual rhythms irrespective of musical beats

ABSTRACT

Music has been shown to entrain movement. One of the body’s most frequent movements, saccades, are arguably subject to a timer that may also be susceptible to musical entrainment. We developed a continuous and highly-controlled visual search task and varied the timing of the search target presentation, it was either gaze-contingent, tap-contingent, or visually-timed. We found: (1) explicit control of saccadic timing is limited to gross duration variations and imprecisely synchronized; (2) saccadic timing does not implicitly entrain to musical beats, even when closely aligned in phase; (3) eye movements predict visual onsets produced by motor-movements (finger-taps) and externally-timed sequences, beginning fixation prior to visual onset; (4) eye movement timing can be rhythmic, synchronizing to both motor-produced and externally timed visual sequences; each unaffected by musical beats. These results provide evidence that saccadic timing is sensitive to the temporal demands of visual tasks and impervious to influence from musical beats.     

Is target movement as well as target displacement a stimulus for saccadic eye movements?

The effects of visual movement on saccadic eye movement have been examined. In a classic apparent-movement demonstration with two successively exposed line-segment targets the quality of the movement is dependent on the relative orientation of the line segments. If saccadic eye movements are elicited between the targets in this situation, the configuration leading to optimal apparent movement also leads to the shortest-latency saccades. When a single line segment is succeeded by two line segments flanking it on opposite sides, and if one of these has the same orientation as the initial one and the other a different orientation, then apparent motion is seen between the two lines with the same orientation. However, the direction of saccades elicited in this configuration is not influenced by the relative orientations of the line segments. The two results together suggest that the effect of visual movement on saccadic eye movement is nonspecific.