Topography of visually evoked brain activity during eye movements: lambda waves, saccadic suppression, and discrimination performance

Abstract

Eye-movement related brain activity was studied in 14 subjects by recording EEG topographically in 16 channels over the occipital brain areas. Potential fields obtained with or without the simultaneous presentation of a visual stimulus during the time course of horizontal saccades were compared. Without visual stimulation, eye movements were followed at a mean latency of about 65 ms by a lateralized occipital dominant component whose topography was determined by the direction of the saccade but whose latency was independent of the time course of the eye movements. This component was reminiscent of lambda waves, however, it could also be elicited in complete darkness. When stimuli were presented during saccades, component latencies increased significantly, and there were also topographic changes in the evoked potential fields. Negative centroids were located more anteriorly and positive ones more posteriorly on the scalp when compared to brain activity recorded with stable eye positions and visual stimulation. All subjects reported no suppression of visual stimuli when presented during saccades occurred. This was confirmed by testing the discrimination performance of an independent group of 27 subjects. Our data show that the execution of saccades elicits electrophysiological patterns of activation in the visual cortex even without visual input. The increase of component latency observed during saccades as well as topographical differences suggest that visual information is processed by different neuronal elements during saccadic eye movements. © 1997 Elsevier Science B.V.

Introduction

In the present paper we will describe how saccadic eye movements influence both electrical brain activity as well as psychophysical performance in a visual pattern discrimination task. As the literature on the neuronal mechanisms of eye movements in humans illustrates, electrical brain activity can be obtained with three different experimental paradigms analyzing: (1) motor activity — related neuronal correlates of eye movements; (2) lambda waves of the EEG following eye movements; and (3) evoked cortical activity modulated by the occurrence of saccades.

As in all motor activity, the planning and execution of saccades is preceded by a `Bereitschaftspotential' (readiness potential) as well as by the neuronal activation of specific areas of the motor cortex (Becker et al., 1972). This potential appears to be identical to what has been termed presaccadic negativity which in part originates in the supplementary motor area that is crucial for the control of self-initiated movements (Moster and Goldberg, 1990; Evdokimidis et al., 1992). In addition, the initiation of saccades is paralleled by activity of neurons in the frontal and supplementary eye fields that has been recorded in animals before and during saccadic eye movements (Schlag and Schlag-Rey, 1987; Goldberg and Bruce, 1990) as well as in humans (Brook-Seidelberg and Adler, 1992). This activity is independent of the so-called spike potential which originates in the eye muscles at the beginning of the saccades (Riemslag et al., 1988).

Following rapid eye movements the spontaneous EEG displays so-called lambda waves that have been reported to originate in occipital areas of the brain (Green, 1957; Scott et al., 1967). Lambda waves have been related to visual information processing triggered by the relative movement of visual features of the visual field across the retina (e.g. Barlow and Ciganek, 1969), and thus, their appearance has been paralleled to the conventional visually evoked potential. Along these lines, we studied the scalp topography of lambda waves that followed spontaneous saccadic eye movements in healthy adults, and we will show that such components are involved in a special kind of visual processing which appears, however, to be independent from incoming visual information and thus is not influenced by the variation of physical stimulus parameters.

For a very long time the term `saccadic suppression' was used in visual psychophysics (Dodge, 1900) which describes the fact that the central processing of visual information is suppressed during rapid eye movements (e.g. Latour, 1962, Volkman, 1962). Visual stimuli flashed during saccades have been described to evoke potentials of reduced amplitude and/or prolonged latency (Gross et al., 1967; Michael and Stark, 1967; Duffy and Lombroso, 1968), and the pupillary response to light stimuli is affected in a similar way (Zuber et al., 1966).

In the present paper we will examine eye movement-related electrical brain activity recorded from 16 electrodes over the occipital cortex in terms of evoked component occurrence and topography. We will not be concerned with activity that is related to the planning or execution phase of saccades but rather: (1) examine the potential role of lambda waves for visual processing; (2) study how visually evoked brain activity is influenced by the execution of saccadic eye movements; and (3) investigate how discrimination performance is affected by saccades.