The Dorsal Attention Network Mediates Orienting toward Behaviorally Relevant Stimuli in Spatial Neglect

Abstract

Experimental neurophysiology and functional neuroimaging have identified a dorsal attention network that encodes neural signals related to the behavioral significance of a stimulus. The core anatomical areas of this network are the frontal eye fields and the posterior parietal cortex, which are interconnected by the superior longitudinal fasciculus. Here, we show that damage or disconnection of this network predicts the extent to which task-relevant stimuli capture attention of human stroke patients with spatial neglect. Healthy volunteers, right-hemisphere-damaged control participants, and patients with left neglect reacted to peripheral targets defined by their color, which were preceded by a brief distracter stimulus. The position of the distracter and its relevance for the current trial were independently varied. In neglect patients with damage including the frontal eye fields and the superior longitudinal fasciculus, ipsilesional distracters impaired orienting into contralesional space regardless of their relevance for the current task. In contrast, patients with sparing of these regions were only impaired when distracters were task-relevant. These findings indicate that the dorsal attention network controls spatial orienting by modulating the saliency of distracter stimuli according to current action goals.

Task relevance effects in electrophysiological brain activity: Early, but not first

“…The inverse solution computed for the relevance effect localized sources of activity in the right intraparietal sulcus (IPS) and neighbouring regions of the PPC, as well as more anterior regions of the frontoparietal convexity. This distribution of activity is compatible with functional imaging and neuropsychological studies demonstrating the involvement of a frontoparietal network in voluntary aspects of attention (Corbetta et al, 2000;Ptak and Schnider, 2010;Serences and Yantis, 2007). However, the IPS also contained sources of activity related to the processing of saliency, in particular for distracters presented in the left hemifield.…”

Synchronization of fronto-parietal beta and theta networks as a signature of visual awareness in neglect

“…These results confirm models according to which disrupted integrity of right-hemisphere frontoparietal networks is a core pathophysiological mechanism in neglect syndrome (Corbetta and Shulman, 2011;Bartolomeo et al, 2012). So far, a disconnection of right fronto-parietal networks in neglect has been demonstrated at the neuroanatomical and neurofunctional level using in-vivo tractography (Thiebaut de Schotten et al, 2005, 2011, lesion mapping (Ptak and Schnider, 2010;Lunven et al, 2015), fMRI (He et al, 2007;Bartolomeo et al, 2012) and resting state networks analysis of MRI and EEG (Baldassarre et al, 2014;Fellrath et al, 2016). However, the role of transient functional synchronization as a network-based mechanism underlying perceptual deficits in neglect has not been identified.…”

“…In this perspective, the impairment of dorsal FP theta networks in neglect patients is consistent with the results of Ptak and Schnider (2010) identifying the dorsal networks as critical, as well as with most recent observations of Fellrath et al (2106), according to which a significant decrease of resting-state theta EEG connectivity predicted impaired target processing in patients with spatial neglect. According to He et al (2007), both dorsal and ventral attentional networks are impaired in acute patients with neglect (tested within 1 month after lesion).…”

“…It has been shown that the functional inhibition of fronto-parietal connections generates an intraoperative neglect-like pattern during a bisection line task in patients undergoing surgery (Thiebaut de Schotten et al, 2005). Using lesion-symptom mapping and fractional anisotropy, specific components of fronto-parietal fibers have been isolated that are responsible for the deficits in modulation of attention by task relevance (Ptak and Schnider, 2010) and for severity of chronic symptoms in neglect (Lunven et al, 2015). By measuring hemodynamic coherent fluctuations in the event-related fMRI signal, He et al (2007) were the first to demonstrate disrupted functional connectivity in fronto-parietal networks in neglect patients, as confirmed recently by analysis of resting state functional connectivity using both MRI (Baldassarre et al, 2014) and highresolution electroencephalographic (EEG) signals (Fellrath et al, 2016).…”

“…The key feature of the task was that both the left and right hemi-fields were stimulated, but stimuli could be classified as targets or non-targets only by integrating information from the two hemi-fields (full-field attention task). Thus, visual awareness was challenged both in a bottom-up way, by stimulating simultaneously the two hemi-fields, and in a top-down way, by attributing task relevance to the information from the two hemi-fields (Vuilleumier et al, 2008;Ptak and Schnider, 2010;Ptak, 2012).…”