Lesion evidence for the critical role of the intraparietal sulcus in spatial attention

Abstract

Based on lesion mapping studies, the inferior parietal lobule and temporoparietal junction are considered the critical parietal regions for spatial-attentional deficits. Lesion evidence for a key role of the intraparietal sulcus, a region featuring prominently in non-human primate studies and human functional imaging studies of the intact brain, is still lacking, probably due to the exceptional nature of isolated intraparietal sulcus lesions. We combined behavioural testing and functional imaging in two patients with a focal intraparietal sulcus lesion sparing the inferior parietal lobule and temporoparietal junction to examine the critical contribution of the intraparietal sulcus to spatial attention. Case H.H. had a focal ischaemic lesion (1.8 cm3) that was confined to the posterior segment of the left intraparietal sulcus, whereas Case N.V. had a partially reversible lesion of the middle segment of the right intraparietal sulcus extending into the superior parietal lobule (13.8 cm3). The performance of these cases was contrasted with five cases with a classical inferior parietal lesion, as well as with a group of 31 age-matched controls. In the behavioural study, the patients performed an orientation discrimination task on a peripheral target (eccentricity 7.6°) that was preceded by a central spatial cue. We manipulated both the cue validity (17% trials with an invalid spatial cue) and the presence of a competing distracter in the visual field contralateral to the target (17% double stimulation trials). The ability of the patients with an intraparietal sulcus lesion to reorient their spatial focus of attention and to select between competing stimuli was impaired for contralesional targets compared with controls, similarly to what we saw in the inferior parietal group. Furthermore, we could observe that the deficit in Case N.V. resolved with regression of the lesion. To further evaluate the correspondence between spatial-attentional deficits and the intraparietal sulcus lesions, we ascertained the functional integrity of the inferior parietal lobule and temporoparietal junction in Case H.H. using event-related functional magnetic resonance imaging with the same task as in the behavioural study. The intraparietal sulcus lesion of this patient did not affect the task-related activation of the inferior parietal lobule or temporoparietal junction. Additionally, a resting-state functional magnetic resonance imaging study in Case H.H. and 62 controls revealed that the lesion in Case H.H. did not affect the topology of the ventral attention network nor the strength of its main inter- and intrahemispheric connections. Our findings demonstrate that the human superior parietal cortex critically contributes to spatially selective attention.