Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study

Abstract

The identification of brain systems contributing to different aspects of visuospatial attention is of both clinical and theoretical interest. Cued target detection tasks provide a simple means to dissociate attentional subcomponents, such as alerting, orienting or reorienting of attention. Event-related functional magnetic resonance imaging (fMRI) was used to study neural correlates of these distinct attentional processes. Volunteers were scanned while performing a centrally cued target detection task. Four different types of trials (no cue, neutral cue, valid cue and invalid cue trials) with targets appearing either in the right or left hemifield were randomly intermixed. Behaviourally, the data provided evidence for alerting, spatial orienting and reorienting of attention. Neurally, the alerting effect was seen in bilaterally increased extrastriatal blood oxygenation level-dependent (BOLD) activity in neutral as compared to no cue trials. Neural correlates of spatial orienting were seen in anterior cingulate cortex, which was more active during valid as compared to neutral cue trials. Neural correlates of reorienting of attention, that is, higher BOLD activity to invalid as compared to validly cued trials were evident in several brain regions including left and right intraparietal sulcus, right temporo-parietal junction and middle frontal gyrus bilaterally. The data suggest that frontal and parietal regions are specifically involved in reorienting rather than orienting attention to a spatial position. Alerting effects were seen in extrastriate regions which suggest that increased phasic alertness results in a top–down modulation of neural activity in visual processing areas.

Introduction

Detection of stimuli in the environment can be improved by advance information on where or when a stimulus will appear. Damage to parietal and frontal cortex, especially in the right hemisphere, impairs attention to stimuli in contralateral space Heilman et al., 2003, Marshall and Fink, 2001, Mesulam, 1981. Neuropsychological studies in patients with parietal lesions have shown that stimulus detection is particularly impaired when misleading advance information is provided such that targets appear at unattended locations Losier and Klein, 2001, Petersen et al., 1989, Posner et al., 1984. These findings suggest that the parietal cortex is rather involved in disengagement of attention than orienting attention to a specific point in space. By contrast, frontal patients are very slow in general in such tasks Petersen et al., 1989, Posner et al., 1987, which suggest that disengagement deficits are specific to parietal lesions.

The contribution of parietal cortex and other areas in visuospatial attention has been the focus of several neuroimaging studies using spatial cueing paradigms Coull and Nobre, 1998, Gitelman et al., 1999, Kim et al., 1999, Nobre et al., 1997. Recently, event-related functional magnetic resonance imaging (fMRI) studies have successfully isolated cue and target-related activity in spatial cueing tasks Corbetta et al., 2000, Hopfinger et al., 2000. On the basis of such work, Corbetta and Shulman (2002) propose two attentional networks mediating the functions of orienting and disengagement of attention. The “orienting network” which is involved in visual selection and working memory is dependent on bilateral activity in intraparietal sulcus and the human homologue of frontal eyefields. Reorienting of attention, on the other hand, is achieved by a second network, which is strongly lateralised to the right temporo-parietal junction and inferior frontal gyrus. In this network, activity emerges with salient, unexpected or rare stimuli Downar et al., 2001, Downar et al., 2002 and modulates activity of the orienting network when stimuli occur outside the current focus of attention.

A right-sided network for attentional shifting is in line with the observation that disengagement deficits are usually stronger in patients with right than left parietal damage (Losier and Klein, 2001, see however, Posner et al., 1987). It has also been shown that spatial deficits after right parietal damage are often concurrent with nonspatial attentional dysfunctions such as reduced alertness. Robertson et al. (1998) demonstrated that increased phasic alertness can alleviate spatial deficits in patients with right parietal lesions, suggesting an interaction or overlap between spatial and nonspatial attentional systems. Given this neuropsychological evidence, it would be interesting to know, whether the same right parietal regions are used for reorienting of attention and alerting in healthy volunteers. Indeed, it has been suggested that reorienting of attention is mainly driven by changes in alertness when a target appears at an unexpected location (Corbetta et al., 2002). There are only few neuroimaging studies that investigate the “alerting network”. While some authors point to a right-sided fronto-parieto-thalamic network Sturm and Willmes, 2001, Sturm et al., 1999, others suggest left lateralised parietal and frontal regions (Coull et al., 2001). The results of these studies are thus controversial and the designs employed did not enable a direct comparison of the neural systems underpinning “alertness” and “reorienting” within one study.

We designed an event-related fMRI experiment to study neural correlates of spatial and nonspatial attentional subcomponents, such as alerting, orienting and reorienting of attention. A cued target detection task (Posner, 1980) was used. In contrast to prior block design or event-related approaches, trials were presented in random order and with short cue–target intervals avoiding confounding strategic effects or contribution of working memory and sustained attention. The task involved no, neutral, valid and invalid cue conditions. Alerting, which is defined here as a state of general readiness which follows the presentation of a warning signal, leads to transient changes in responsiveness to incoming information. Alerting was captured by comparing BOLD activity in neutrally cued trials with no cue trials. Orienting involves allocation of attention to a location in space when a spatially informative cue is given and was identified by comparing validly cued trials with neutrally cued trials. Disengagement of attention and reorienting to a new location is necessary upon target presentation when misleading spatial information was provided by the cue. Neural correlates of this process were isolated by comparing invalidly cued trials with validly cued trials. Given the lateralised attentional deficits in patients with neglect, a further aim of the study was to determine whether the different cueing conditions are modulated differentially by the hemifield of target presentation.