Integrated effect of stimulation at fixation points on EFRP (eye-fixation related brain potentials)

doi:10.1016/S0167-8760(99)00010-0

International Journal of Psychophysiology

Volume 32, Issue 3, 1 June 1999, Pages 193-203

https://doi.org/10.1016/S0167-8760(99)00010-0 Get rights and content

Abstract

The purpose of this study was to investigate the integrated effect of stimulation at the fixation points just before and just after saccadic eye-movement (saccade) on eye-fixation related brain potentials (EFRP: P75 and N105). Checkerboard patterns were used as stimuli. In Experiment 1, changes in check sizes between two fixation points enhanced the amplitude of P75, while changes in the phases of patterns between the two points did not affect EFRP. This result showed that EFRP was affected by two fixation points, and that changes in the retinal image between the two points did not necessarily affect EFRP. In Experiment 2, the relationship between EFRP and check size was investigated in detail. A second order relationship between logarithm of check size and the latency of P75, and a linear relationship between logarithm of check size and the amplitude of N105 were found. The effect of check size on the amplitude of P75 which might explain the increased amplitude of P75 observed in Experiment 1 did not appear. These results suggest that EFRP might reflect relative higher processing than peripheral stimulation at one fixation point.

Introduction

In order to perceive the visual world, we make saccadic eye-movements (saccade) from one fixation point to another. When EEGs time-locked to the offset of saccades are averaged, eye-fixation related brain potentials (EFRP) can be obtained (Yagi, 1995). EFRP consist of several components. The most prominent component of EFRP is a large positive deflection with a peak latency of approximately 80 ms from the offset of the saccade. This is called the lambda response. Scott et al. (1981)examined the lambda response by averaging EEGs at onset of saccades. However, Yagi, 1979, Yagi, 1981afound that the lambda response was linked to the offset of the saccade; i.e. the onset of eye-fixation. Other studies also support this finding (Szirtes et al., 1982, Billings, 1989, Jagla and Zikmund, 1994). Since suppression occurs during saccades (e.g. Zuber and Stark, 1966, Matin, 1974, Volkmann, 1986), the lambda response is thought to be evoked by the inflow of visual information after termination of the saccade.

The lambda response like the so-called visual evoked potentials (VEP) is influenced by physical and psychological factors. For instance, the latency and amplitude of lambda responses vary with the size of the saccade (Kurtzberg and Vaughan, 1977, Yagi, 1979), the arousal/attentional level of subjects (Yagi, 1981b), and the physical properties of stimulus such as its luminance (Gaarder et al., 1964) and contrast (Yagi et al., 1992). The latency and amplitude of lambda responses vary with stripe width in striped patterns (Yagi et al., 1993).

Several authors (Scott et al., 1981Riemslag et al., 1987Billings, 1989) have found similarities between the lambda response and pattern VEP in the same subject. These studies support the idea that lambda response can be a useful index of visual information processing as well as the VEP.

When we view a picture or read sentences, for example, visual perception ordinarily consists of more than one fixation point. Visual information obtained at each eye fixation point is integrated into a perception. Therefore, the lambda response may be influenced by not only the stimulus at the fixation following the saccade, but also by the stimulus at the fixation prior to the saccade. For example, Yagi (1987)found a significant correlation between fixation duration and the amplitude of the lambda wave at the next fixation, in a case study with a subject who showed large lambda waves in raw EEGs. Kurtzberg and Vaughan (1977)postulated that the lambda response might represent a fusion of activity generated by stimulus at both the onset and offset points of the saccade. Yagi (1979)and Thickbroom et al. (1991)suggested that the lambda response might be the compound of an onset related component and an offset related component. These studies, however, did not directly investigate the relationship between stimuli at the onset and at the offset of the saccade. The purpose of the present study was to investigate the integrated effect of stimuli at both the onset and offset of the saccade on EFRP using checkerboard patterns as stimuli.

Section snippets

Experiment 1

The purpose of Experiment 1 was to examine the integrated effect of the stimuli at two fixation points (onset point and offset point of the saccade) on EFRP. Two properties of the checkerboard patterns; i.e. the check sizes (30′ and 120′) and the phase differences (congruent and reversal), were varied under six conditions. Under the congruent conditions, the two patterns presented at onset and offset of the saccade had the same alignment of black and white elements. Under the reversal

Experiment 2

Little attention has been paid to the effect of check size on lambda response or EFRP. The purpose of Experiment 2 was to examine the effect of check size on P75 (lambda response) and N105. Check sizes were 30′, 45′, 60′, 90′ and 120′. This examination might clarify the effect on EFRP by the different check sizes between two fixation points which was observed in Experiment 1.

General discussion

The purpose of the present study was to examine whether EFRP (P75 and N105) reflect visual information processing at only one or more than one fixation point, by using checkerboard patterns as stimuli.

In Experiment 1, the check sizes and the phases of the stimuli were manipulated. The change in the check sizes between the two points enhanced the amplitude of P75. This result proved that EFRP reflects visual information processing at more than one fixation point. The change in phases between the

Acknowledgements

The present study is supported by MITI (Ministry of International Trade and Industry) and NEDO (the New Energy and Industrial Technology Development Organization)'s Project on `Human Sensory Measurement Application Technology'.

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One of the most prominent components of EFRPs is the lambda response. This is a positive deflection occurring around 80 ms from the onset of a fixation (Kazai and Yagi, 2003)and has been shown to vary depending on the properties of the visual stimuli and attention (Kazai and Yagi, 1999). As such we were particularly interested in determining any differences in EFRPs between our high and low cognitive load conditions for the period 50−150 ms after the onset of fixations.
Previous research has demonstrated that the distraction caused by holding a mobile telephone conversation is not limited to the period of the actual conversation (Haigney, 1995; Redelmeier & Tibshirani, 1997; Savage et al., 2013). In a prior study we identified potential eye movement and EEG markers of cognitive distraction during driving hazard perception. However the extent to which these markers are affected by the demands of the hazard perception task are unclear. Therefore in the current study we assessed the effects of secondary cognitive task demand on eye movement and EEG metrics separately for periods prior to, during and after the hazard was visible. We found that when no hazard was present (prior and post hazard windows), distraction resulted in changes to various elements of saccadic eye movements. However, when the target was present, distraction did not affect eye movements.
We have previously found evidence that distraction resulted in an overall decrease in theta band output at occipital sites of the brain. This was interpreted as evidence that distraction results in a reduction in visual processing. The current study confirmed this by examining the effects of distraction on the lambda response component of subjects eye fixation related potentials (EFRPs). Furthermore, we demonstrated that although detections of hazards were not affected by distraction, both eye movement and EEG metrics prior to the onset of the hazard were sensitive to changes in cognitive workload. This suggests that changes to specific aspects of the saccadic eye movement system could act as unobtrusive markers of distraction even prior to a breakdown in driving performance.
Improving free-viewing fixation-related EEG potentials with continuous-time regression
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The shape of this distortion will be hard to predict, due to the fluctuating shape of the overlapping responses. The fourth issue, the relationship between eye movement parameters and neural activity, can be a subject of study in its own right (Kazai and Yagi, 1999; Nikolaev et al., 2016; Thickbroom et al., 1991). When it is not, differing EMs can confound EEG comparisons.
In the analysis of combined ET-EEG data, there are several issues with estimating FRPs by averaging. Neural responses associated with fixations will likely overlap with one another in the EEG recording and neural responses change as a function of eye movement characteristics. Especially in tasks that do not constrain eye movements in any way, these issues can become confounds.
Here, we propose the use of regression based estimates as an alternative to averaging. Multiple regression can disentangle different influences on the EEG and correct for overlap. It thereby accounts for potential confounds in a way that averaging cannot. Specifically, we test the applicability of the rERP framework, as proposed by Smith and Kutas (2015b), (2017), or Sassenhagen (2018) to combined eye tracking and EEG data from a visual search and a scene memorization task.
Results show that the method successfully estimates eye movement related confounds in real experimental data, so that these potential confounds can be accounted for when estimating experimental effects.
The rERP method successfully corrects for overlapping neural responses in instances where averaging does not. As a consequence, baselining can be applied without risking distortions. By estimating a known experimental effect, we show that rERPs provide an estimate with less variance and more accuracy than averaged FRPs. The method therefore provides a practically feasible and favorable alternative to averaging.
We conclude that regression based ERPs provide novel opportunities for estimating fixation related EEG in free-viewing experiments.
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Systematic differences in eye movement characteristics thus act as potential confounds and require careful control (Dimigen et al., 2011; Nikolaev et al., 2016). Therefore, early EEG- and eye movement co-registration studies focused on the saccadic spike and lambda potential using controlled saccadic tasks (e.g., Kazai & Yagi, 1999, 2003; Thickbroom, Knezevič, Carroll, & Mastaglia, 1991; Thickbroom & Mastaglia, 1986). More recent investigations have shown, however, that it is possible to obtain longer-latency FRP components which provide insight into cognitive mechanisms even in unrestricted eye movement behavior.
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.
Combining EEG and eye movement recording in free viewing: Pitfalls and possibilities
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Thus, EFRP is a hybrid construct, combining an exploration-driven, eye movement induced signal with a stimulus-driven one, the potential evoked by the visual features at fixation. EFRPs during both controlled and free eye movement behavior have been studied for several decades (Billings, 1989b; Devillez, Guyader, & Guerin-Dugue, 2015; Dimigen et al., 2011; Fudali-Czyz, Francuz, & Augustynowicz, 2014; Kazai & Yagi, 1999; Körner et al., 2014; Nikolaev et al., 2011; Rama & Baccino, 2010; Thickbroom et al., 1991; Yagi, 1979). Since EFRPs have such a venerable history, we will adopt its terminology for describing the time-frequency EEG activity around a saccade.
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.
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Despite the compelling contribution of the study of event related potentials (ERPs) and eye movements to cognitive neuroscience, these two approaches have largely evolved independently. We designed an eye-movement visual search paradigm that allowed us to concurrently record EEG and eye movements while subjects were asked to find a hidden target face in a crowded scene with distractor faces. Fixation event-related potentials (fERPs) to target and distractor stimuli showed the emergence of robust sensory components associated with the perception of stimuli and cognitive components associated with the detection of target faces. We compared those components with the ones obtained in a control task at fixation: qualitative similarities as well as differences in terms of scalp topography and latency emerged between the two. By using single trial analyses, fixations to target and distractors could be decoded from the EEG signals above chance level in 11 out of 12 subjects. Our results show that EEG signatures related to cognitive behavior develop across spatially unconstrained exploration of natural scenes and provide a first step towards understanding the mechanisms of target detection during natural search.
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When we measure the visual event-related potential (ERP), a subject has to fix eyes to a point on the display in an experimental situation or in a diagnosis on the visual function. Therefore, it is very hard to apply the event-related potential (ERP) to assessment of sensation and attention at clinical fields or at industrial settings. We developed a system to analyze the brain potential associated with offset of saccadic eye movements. The potential is called eye fixation-related potential (EFRP). EFRP is identical with the so-called visual ERP. We can measure the topographical change of EFRP in real time. The first system with a UNIX (Version 1) was very fast, but very expensive. However, the new system (Version 2) is more economical, because it can be used in a notebook computer with Windows XP. EEG and EOG data can be sampled in real time, although the data are analyzed offline. The new system will be useful to study cognitive factors under eye movement conditions.

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Integrated effect of stimulation at fixation points on EFRP (eye-fixation related brain potentials)

Abstract

Introduction

Section snippets

Experiment 1

Experiment 2

General discussion

Acknowledgements

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Brain Res.

Vision Res.

Electroencephalogr. Clin. Neurophysiol.

Int. J. Psychophysiol.

Electroencephalogr. Clin. Neurophysiol.

Exp. Neurol.

Averaged brain activity following saccadic eye movement

Science