EEG studies in healthy humans have highlighted that alpha-band activity is relatively reduced over the occipital–parietal areas of the hemisphere contralateral to the direction of spatial attention. Here, we investigated the hemispheric distribution of alpha during orienting of attention in male and female right brain-damaged patients with left spatial neglect. Temporal spectral evolution showed that in patients with neglect alpha oscillations over the damaged hemisphere were pathologically enhanced both during the baseline-fixation period that preceded cued orienting (capturing tonic alpha changes) and during orienting with leftward, rightward, or neutral-bilateral spatial cues (reflecting phasic alpha changes). Patients without neglect showed a similar though significantly less enhanced hemispheric asymmetry. Healthy control subjects displayed a conventional decrease of alpha activity over the hemisphere contralateral to the direction of orienting. In right-brain-damaged patients, neglect severity in the line bisection task was significantly correlated both with tonic alpha asymmetry during the baseline period and with phasic asymmetries during orienting of attention with neutral-bilateral and leftward cues. Asymmetries with neutral-bilateral and leftward cues were correlated with lesion of white matter tracts linking frontal with parietal–occipital areas. These findings show that disruption of rostrocaudal white matter connectivity in the right hemisphere interferes with the maintenance of optimal baseline tonic levels of alpha and the phasic modulation of alpha activity during shifts of attention. The hemispheric distribution of alpha activity can be used as a diagnostic tool for acquired pathological biases of spatial attention due to unilateral brain damage.SIGNIFICANCE STATEMENTAlpha desynchronization over the hemisphere contralateral to the attended side of space is a reliable marker of attentional orienting in the healthy human brain: can the same marker be used to spot and quantify acquired disturbances of spatial attention after unilateral brain injuries? Are pathological modifications in the hemispheric distribution of alpha specifically linked to attentional neglect for one side of space? We show that in patients with right brain damage the pathological enhancement of alpha oscillations over the parietal and occipital areas of the injured hemisphere is correlated with reduced awareness for the left side of space and with the lesion of white matter pathways that subserve frontal modulation of alpha activity in posterior brain areas.

Studies with event-related potentials have highlighted deficits in the early phases of orienting to left visual targets in right-brain-damaged patients with left spatial neglect (N+). However, brain responses associated with preparatory orienting of attention, with target novelty and with the detection of a match/mismatch between expected and actual targets (contextual updating), have not been explored in N+. Here in a study in healthy humans and brain-damaged patients of both sexes we demonstrate that frontal activity that reflects supramodal mechanisms of attentional orienting (Anterior Directing Attention Negativity, ADAN) is entirely spared in N+. In contrast, posterior responses that mark the early phases of cued orienting (Early Directing Attention Negativity, EDAN) and the setting up of sensory facilitation over the visual cortex (Late Directing Attention Positivity, LDAP) are suppressed in N+. This uncoupling is associated with damage of parietal-frontal white matter. N+ also exhibit exaggerated novelty reaction to targets in the right side of space and reduced novelty reaction for those in the left side (P3a) together with impaired contextual updating (P3b) in the left space. Finally, we highlight a drop in the amplitude and latency of the P1 that over the left hemisphere signals the early blocking of sensory processing in the right space when targets occur in the left one: this identifies a new electrophysiological marker of the rightward attentional bias in N+. The heterogeneous effects and spatial biases produced by localized brain damage on the different phases of attentional processing indicate relevant functional independence among their underlying neural mechanisms and improve the understanding of the spatial neglect syndrome.SIGNIFICANCE STATEMENTOur investigation answers important questions: are the different components of preparatory orienting (EDAN, ADAN, LDAP) functionally independent in the healthy brain? Is preparatory orienting of attention spared in left spatial neglect? Does the sparing of preparatory orienting have an impact on deficits in reflexive orienting and in the assignment of behavioral relevance to the left space? We show that supramodal preparatory orienting in frontal areas is entirely spared in neglect patients though this does not counterbalance deficits in preparatory parietal-occipital activity, reflexive orienting, and contextual updating. This points at relevant functional dissociations among different components of attention and suggests that improving voluntary attention in N+ might be behaviorally ineffective unless associated with stimulations boosting the response of posterior parietal-occipital areas.