Elsevier

NeuroImage

Volume 22, Issue 1, May 2004, Pages 304-314
NeuroImage

The encoding of saccadic eye movements within human posterior parietal cortex

https://doi.org/10.1016/j.neuroimage.2003.12.039Get rights and content

Abstract

Over the last few years, several functionally distinct subregions of the posterior parietal cortex (PPC) have been shown to subserve oculomotor control. Since these areas seem to overlap with regions whose activation is related to attention, we used functional magnetic resonance imaging to compare the cerebral activation pattern evoked by eye movements with different attentional loads, i.e., oscillatory saccades with different frequencies, as well as predictable, and unpredictable saccades. Our results show activation in largely overlapping networks with differing strength of activity and symmetry of involved areas. Predictable saccades having the shortest saccadic latency led to the most pronounced cerebral activity both in terms of cortical areas involved and signal intensity. Predictable and unpredictable saccades were dominated by activation within the right hemisphere, whereas oscillatory saccades showing the longest saccadic latency were dominated by activation within the left hemisphere. In all tasks, the centers of gravity of activation occurred within the posterior part of the intraparietal sulcus (IPS), while the predictable saccades additionally activated its anterior part. The enhanced activity during the execution of predictable saccades was probably related to top-down processing and/or the preparation of the upcoming eye movement. The hemispheric difference could arise from a predominant role of the right PPC for shifting spatial attention and the left PPC for shifting temporal attention. The differential encoding of saccadic eye movements within IPS indicates that the PPC splits up into different functional modules related to the particular demands of a saccade.

Introduction

The cortical regions associated with the execution of eye movements were first demonstrated in the pioneering experiments of Ferrier (1874), who elicited saccadic eye movements by electrical stimulation of the monkey brain. The following century yielded a specification of the oculomotor circuitry with electrophysiological studies in nonhuman primates Barash et al., 1991, Bruce and Goldberg, 1985, Schiller and Chou, 1998, Schlag and Schlag-Rey, 1987, Schlag et al., 1998, clinical studies in humans Gaymard and Pierrot-Deseilligny, 1999, Gaymard et al., 1998, Heide and Kömpf, 1998, Pierrot-Deseilligny et al., 1997, and recent functional imaging studies Corbetta et al., 1998, Darby et al., 1996, Kimmig et al., 2001, Luna et al., 1998, O'Driscoll et al., 1995, Rosano et al., 2002. From these studies, three main areas in the human cortex emerged that are dedicated to the control of saccades: the frontal eye field (FEF), the supplementary eye field (SEF), and the (putative) parietal eye field. While FEF (Paus, 1996) and SEF (Grosbras et al., 1999) are well defined in terms of localization and functional implication, the role of the saccade-related regions in the PPC remains to be further clarified. The determination of saccade-related areas is complicated by the tight connections between attention and oculomotor processes within PPC Büchel et al., 1998, Corbetta, 1998, Nobre et al., 2000, Rizzolatti et al., 1987.

The main goal of this study was, therefore, to describe the neural activation in the human PPC associated with saccadic eye movements differing in their spatial and temporal predictability. Additionally, we wanted to elucidate the influence of cognitive factors on the activation pattern during the execution of saccades. We aimed at exploring the question whether predictable saccades comprising endogenous shifts of attention and preparation of the upcoming eye movement show a different cortical activation pattern than reactive or oscillatory saccades. Here we report on the particular role of cortical areas along the intraparietal sulcus (IPS) for the control of saccades of different predictability. Preliminary data were presented in abstract form (Konen et al., 2002).

Section snippets

Subjects

Eleven healthy right-handed subjects (three males, eight females, mean age 22.6 years, range 19–27) participated in the study. Handedness was assessed with the “Edinburgh Handedness Inventory” (Oldfield, 1971). All subjects had normal or corrected to normal vision and had no history of neurological or psychiatric diseases. Informed consent was obtained from each subject before the experiments started, which were approved by the “Ethic Committee of the Heinrich-Heine-University”.

Scanning sequences

Functional

Behavioral data

The mean latencies for predictable saccades were 136 ms (standard deviation = 65 ms) and for unpredictable saccades 194 ms (standard deviation = 47 ms). The mean latencies for high-frequency saccades were 210 ms (standard deviation = 82 ms) and for low-frequency saccades 254 ms (standard deviation = 65 ms). The mean latencies between the conditions were significantly different (two-way ANOVA, p < 0.01), whereas the mean data between subjects differed not significantly. Both predictable and

Reaction times

The saccadic latencies differed between the tasks. Predictable saccades elicited the fastest reaction time and the highest proportion of express saccades (for review, see Fischer and Weber, 1993). We ascribe the discrepancy of latencies to the crucial role of the valid cue. When a subject has advanced knowledge about an impending eye movement, the reduced reaction time is thought to reflect the partial or complete preparation of the respective saccade and/or the allocation of attention.

Acknowledgements

This research was supported by HFSP (RG0149/1999-B) and SFB 194 (A 13). The authors thank Erika Raedisch for excellent technical assistance.

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