Time course of cross-hemispheric spatial updating in the human parietal cortex

Abstract

In human parietal cortex, the retinal location of a just seen visual stimulus is updated from one hemisphere to the other, when a horizontal eye movement brings the representation of the stimulus into the opposite visual hemifield. The present study aimed to elucidate the time course of this process. Twelve subjects performed an updating task, in which a filled circle was shown before a horizontal saccade, requiring updating of stimulus location, and a control task without visual stimulation before the saccade. Electroencephalogram (EEG) and electrooculogram (EOG) were recorded while subjects performed the tasks and LORETA source analysis was performed on event-related potential (ERP) components. ERP amplitudes were more positive in the updating condition in comparison to the control condition in two latency windows. An early positive wave starting at about 50 ms after saccade offset and originating in the posterior parietal cortex contralateral to saccade direction probably reflects the integration of saccade-related and visual information and thus the updating process. A shift of the representation of the to-be-updated stimulus to the opposite hemisphere is reflected in a later component starting approximately 400 ms after saccade offset, which is related to memory and originates in the PPC ipsilateral to saccade direction and thus contralateral to the spatial location of the updated visual stimulus.

Introduction

To maintain a stable perception of the world, the visual system has to account for the retinal consequences of eye movements [8]. An efference copy signal of the command to move the eyes is thought to underlie the so-called updating process [3], [40], [46]. FMRI studies in humans and single-cell recordings in monkeys have shown that the posterior parietal cortex plays a critical role in this process [10], [19], [23], [27], [29], [30], [44].

On a single-cell level, the time course of the updating process has been established. In the monkey lateral intraparietal area (LIP) neurons have been found, which show predictive visual processing [10]. Around the time of a saccade, these neurons respond to visual stimuli in their post-saccadic receptive field earlier than would be expected from latencies in a fixation task. Some neurons even respond before saccade onset, corroborating the assumption that a signal corollary to the saccade command is responsible for updating. Such predictive responses were also observed in the frontal eye field (FEF) [45]. It has also been shown that some LIP neurons respond, when the location of a previously flashed stimulus is brought into their receptive field by a saccade, even if the stimulus has already disappeared [10]. The response associated with memory of a stimulus in the future receptive field can also be predictive, i.e., occur earlier than a response to a visual stimulus would be expected in a fixation task [23].

In a recent fMRI study, it was shown that in humans, similar to monkeys, cortical activation in response to visual stimuli can be distinguished from a saccade-locked response to the memory trace of a visual stimulus. While the presentation of lateral visual stimuli mainly causes activation of contralateral striate, extrastriate and parietal cortex [9], [35], an ipsilateral response occurs in parietal cortex, when a saccadic eye movement brings the location of the visual stimulus into the opposite visual hemifield, even if the stimulus is no longer present [30]. Visual information is thus continuously updated in parietal cortex in humans with each eye movement, providing a gaze-centered representation of visual space [29]. Although Merriam et al. [30] reported that the response to the memory trace is time-locked to the saccade rather than to the presentation of the visual stimulus, the precise timing of the updating process is as yet unclear. Given the findings on predictive visual responses in the monkey, it is possible that the response to the memory trace of a visual stimulus in human parietal cortex is also predictive.

So far, only a few studies have examined temporal aspects of updating of visual space in humans. Event-related potential (ERP) components between 70 ms and 120 ms after saccade onset have been observed in conjunction with single horizontal saccades and are discussed in terms of an efference copy signal of the just executed eye movement reaching the occipito-parietal cortex [1], [22], [37]. When subjects perform a saccadic double-step task, which requires the use of efference copy information about the first saccade to perform a correct second saccade, updating takes place in the inter-saccade interval [4]. However, perceptual updating associated with a single saccade may have a different time course. This is supported by single cell recordings in the monkey area LIP. While predictive remapping, as described above, has been observed when visual stimuli are shown around the time of a single saccade, LIP neurons seem to code for the next planned saccade in a saccade sequence [27].

Using a procedure similar to the fMRI study by Merriam et al. [30], the present study aimed to elucidate the time course of cross-hemispheric updating in conjunction with a single horizontal saccade in humans by assessing the response to the memory trace of a visual stimulus using event-related potentials. More specifically, it was aimed to examine whether the time course of cross-hemispheric updating reflected predictive visual processing.