Right-sided parietal lesions lead to lateralized attentional deficits which are most prominent with bilateral stimulation. We determined how an irrelevant stimulus in the unattended hemifield alters attentional responses in parietal cortex during unilateral orienting. A trial consisted of a central spatial cue, a delay and a test phase during which a grating was presented at 9 degrees eccentricity. Subjects had to discriminate the orientation of the grating. The unattended hemifield was either empty or contained a second, irrelevant grating. We carried out a series of functional MRI (fMRI) studies in 35 healthy volunteers (13 men and 22 women, aged between 19 and 30 years) as well as a behavioural and structural lesion mapping study in 17 right-hemispheric lesion patients, 11 of whom had neglect. In the patients with but not in those without neglect, the addition of a distractor in the unattended hemifield significantly impaired performance if attention was directed contralesionally but not if it was directed ipsilesionally. In the healthy volunteers, we discerned two functionally distinct areas along the posterior-anterior axis of the intraparietal sulcus (IPS). The posterior, descending IPS segment in both hemispheres showed attentional enhancement of responses during contralateral attentional orienting and was unaffected by the presence of an irrelevant stimulus in the ignored hemifield. In contrast, the right-sided horizontal IPS segment showed a strong attentional response when subjects oriented to a stimulus in the relevant hemifield and an irrelevant stimulus was simultaneously present in the ignored hemifield, compared with unilateral stimulation. This effect was independent of the direction of attention. The symmetrical left-sided horizontal IPS segment showed the highest responses under the same circumstances, in combination with a contralateral bias during unilateral stimulation conditions. None of the six patients without neglect had a lesion of the horizontal IPS segment. In four of the 11 neglect patients, the lesion overlapped with the horizontal IPS activity cluster and lay in close proximity to it in another four. The remaining three patients had a lesion at a distance from the parietal cortex. Our findings reconcile the role of the IPS in endogenous attentional control with the clinically significant interaction between direction of attention and bilateral stimulation in right parietal lesion patients. Functional imaging in neglect patients will be necessary to assess IPS function in those cases where the structural lesion spares the middle IPS segment.