Functional anatomy of a prelearned sequence of horizontal saccades in humans

Abstract

We have used positron emission tomography (PET) to study the functional anatomy of the repetition of a prelearned sequence of horizontal saccadic eye movements. Five subjects had to memorize a sequence of six successive horizontal saccades. The subjects were scanned in total darkness under three different conditions: at rest, during the execution of self-paced horizontal saccades, and while repeating a prelearned saccades sequence. The repetition of the prelearned saccades sequence led to specific normalized regional cerebral blood flow (NrCBF) increases at the depth of the superior frontal sulcus as well as at the rostral part of the supplementary motor area, whereas at the parietal level an important activation was observed in the intraparietal sulcus extending up to the precuneus. In addition, it was noticed that compared with the resting control condition, both oculomotor tasks activated a common set of cortical and subcortical areas. At the cortical level, this network was composed of the frontal eye fields, the supplementary eye fields, the median part of the cingulate gyrus, and the insula. At the subcortical level, the lenticular nucleus and the thalamus as well as the cerebellar vermis were activated consistently. A direct comparison of our results with those of other PET studies on spatial vision suggest that the dorsal visuospatial pathway could be extended toward the frontal premotor region. In such a scheme, visuospatial information computed in the intraparietal sulcus would be transmitted to the frontal premotor cortex to optimize a spatial-oriented behavior. This is consistent with the early proposal that perceptual and intentional components of spatial information are mediated through superior parietal and frontal areas, respectively.

Fig. 1.

Sample of horizontal EOG recordings in one subject (S5) during the three conditions. E, Eye movements;T, target position along a horizontal axis; R, right; L, left.

Fig. 2.

Detailed analysis of the EOG recorded during the prelearned saccades sequences that each subject had to memorize (shaded bars) and the averaged sequences that were executed (open bars).

Fig. 3.

SPMs for three comparisons. A,SEQ versus REST; B, SAC versus REST;C, SEQ versus SAC. Significant pixels at the given threshold of p < 0.001 uncorrected for multiple comparisons are displayed on single sagittal, coronal, and axial projections of the brain. The spatial location of each activated area can be established by comparing its position in the three views:AC-PC, anterior commissure-posterior commissure plane;VAC, VPC, vertical plane passing through the anterior and posterior commissure, respectively.

Fig. 4.

HMSD results for subjects S1 and S2 when the repetition of prelearned saccades sequences was compared directly with the resting control condition. After alignment of the MRI and PET volumes in the same coordinates space, the different detected objects are superimposed on their corresponding axial MRI slice for each subject. A detailed anatomical analysis after sulcal identification allows accurate localization of these activations. Superior frontal sulcus (yellow); intraparietal sulcus (white);Ro, Rolandic sulcus; Pr, precentral sulcus;Po, postcentral sulcus; R, right; L, left; AC-PC +x mm, axial plane x mm above the bicommissural plane. Details of the detected objects are given in Results.

Fig. 5.

HMSD results for subjects S3 and S5 when the repetition of prelearned saccades sequences was compared directly with the resting control condition. See Figure 4 legend for details.