Elsevier

NeuroImage

Volume 26, Issue 2, June 2005, Pages 471-479
NeuroImage

The activation of attentional networks

https://doi.org/10.1016/j.neuroimage.2005.02.004Get rights and content

Abstract

Alerting, orienting, and executive control are widely thought to be relatively independent aspects of attention that are linked to separable brain regions. However, neuroimaging studies have yet to examine evidence for the anatomical separability of these three aspects of attention in the same subjects performing the same task. The attention network test (ANT) examines the effects of cues and targets within a single reaction time task to provide a means of exploring the efficiency of the alerting, orienting, and executive control networks involved in attention. It also provides an opportunity to examine the brain activity of these three networks as they operate in a single integrated task. We used event-related functional magnetic resonance imaging (fMRI) to explore the brain areas involved in the three attention systems targeted by the ANT. The alerting contrast showed strong thalamic involvement and activation of anterior and posterior cortical sites. As expected, the orienting contrast activated parietal sites and frontal eye fields. The executive control network contrast showed activation of the anterior cingulate along with several other brain areas. With some exceptions, activation patterns of these three networks within this single task are consistent with previous fMRI studies that have been studied in separate tasks. Overall, the fMRI results suggest that the functional contrasts within this single task differentially activate three separable anatomical networks related to the components of attention.

Introduction

The study of attention has been important for the integration of cognitive approaches with neuroscience (Desimone and Duncan, 1995, Kastner and Ungerleider, 2000, Miller and Cohen, 2001, Posner, 2004, Posner and Petersen, 1990). There is widespread agreement from imaging (Corbetta et al., 2000, Kastner et al., 1999) and cellular recording studies (Desimone and Duncan, 1995) that orienting to sensory information activates a common network of neural areas even before a target is presented. This suggests that there is a specific network that serves as the source of the enhancement of neural signals related to processing a target. Similarly, neuroimaging studies have revealed a specific network of areas that relate to obtaining the alert state (Coull et al., 1996, Pardo et al., 1991, Posner and Petersen, 1990) and to resolving conflict among responses (Botvinick et al., 1999, MacDonald et al., 2000). However, each of these forms of evidence comes from separate experiments each with unique task demands, which precludes direct examination of the separability of these networks within the same task.

We developed an attention network test (ANT) to provide a behavioral measure of the efficiency of the three attentional networks within a single task (Fan et al., 2002). The ANT is designed to provide an overall assay with the minimum number of trials. It does not use a validity manipulation of cues. However, the ANT provides outcome measures that indicate the efficiency of the networks that perform the alerting, orienting, and executive (conflict resolution) functions of attention. Since our original report, the ANT has been widely used as a behavioral test to assay performance of normal children (Mezzacappa, 2004, Rueda et al., 2004) and those with disorders (Bish et al., 2005, Sobin et al., 2004), adults with borderline personality disorder compared to temperamentally matched controls (Klein, 2003, Posner et al., 2002), and patients with schizophrenia (Wang et al., in press) and with Alzheimer's disease (Fernandez-Duque and Black, in press). Other studies of autism, attention deficit disorder, mild traumatic brain injury, and the effects of training are also in progress.

In addition, we have shown that the conflict network is highly heritable (Fan et al., 2001). Performance in resolving conflict using the ANT relates to two dopamine genes (Fossella et al., 2002). Although exactly how and where these genes influence dopamine release is not clear, alleles of the DRD4 and MAOA gene did show differential activation of the anterior cingulate in a study using fMRI (Fan et al., 2003b). Interestingly, MAOA alleles that are predicted to result in higher levels of extra-synaptic dopamine did not show associations with more efficient cognition, but rather were associated with less efficient executive attention performance. These results stand in contrast with other studies that combine imaging and genetics to explore individual differences where alleles that predict higher levels of DA were associated with more efficient executive function (Egan et al., 2001, Mattay et al., 2003).

In our original report of work with the ANT (Fan et al., 2002), we found there was a good deal of support for independence between networks. This was shown by the lack of correlation between the scores obtained for each network and the existence of only two small interactions in which the no cue and spatial cue conditions both reduced the degree of conflict. In a larger sample study using the ANT (Fossella et al., 2002), we have found a small but significant negative correlation between the alerting and conflict scores. Moreover, with specific changes to the paradigm, additional interactions between the network scores have been observed. For example, in a study using a tone for the alerting signal and manipulating validity of the visual cue, it was found that the alerting network inhibits the executive network and the orienting network enhances the executive network (Callejas et al., 2004). Although the original configuration of the ANT demonstrated independence of the networks, it would be surprising if the networks did not communicate and thus influence each other with other task demands. Although previous imaging studies suggest that the networks of neural areas serving as the sources of the orienting, alerting, and conflict effects are anatomically separable, there is substantial functional overlap. The most extensive data are on an orienting network that includes the superior parietal lobe, temporal parietal junction, and frontal eye field (Corbetta and Shulman, 2002). Sometimes these effects have been thought to be due to a shift of the focus of attention to the target location and they have also sometimes been thought of as a change of focal length to incorporate a larger area. By comparing a peripheral cue with a small central cue we attempt to encourage a shift of attention to the new location. In support of this idea, we found the spatial cue condition to reduce the flanker effect as though a smaller focus of attention is obtained when the person is specifically cued to the center arrow (Fan et al., 2002).

There are data relating the norepinephrine network to alerting that include thalamic, frontal, and parietal areas (Coull et al., 1996, Marrocco and Davidson, 1998, Posner and Petersen, 1990). Imaging studies of the executive network involved in the control of conflict have consistently activated areas of the dorsal anterior cingulate and often the lateral prefrontal cortex (Bush et al., 2000, MacDonald et al., 2000). However, these results were obtained in separate studies, with methods that differ from those of the ANT, therefore the extent of anatomical separation is not known. It is important to see the extent to which these previous imaging results apply to the ANT, where the three networks are activated in a single study designed to maximize their functional independence in order to determine separation and overlap in the functional anatomy of the three networks.

The present study attempted to isolate the neural networks responsible for performance on the three indices of the ANT. To most directly test the separability of these three networks, we took advantage of the unique design of the ANT to measure these effects within the same group of subjects during performance of the same blocks of scanning. We ran an event-related fMRI experiment using the ANT to find brain areas active for the three attentional networks. We hypothesized that a pattern of separable activity would emerge with specific attentional functions loading heavily on segregated anatomical areas. We explored the following specific hypotheses based on previous studies that have isolated each network within separate tasks on separate subjects: (1) alerting would activate the frontal and parietal areas of the right and/or left hemisphere and thalamic areas that are potentially related to norepinephrine (Coull et al., 2000, Coull et al., 2001, Marrocco and Davidson, 1998). Early neuroimaging and lesion studies together with evidence of a right hemisphere bias in NE have suggested a right hemisphere basis for sustained attention (see Posner and Petersen, 1990 for a summary). However, more recent fMRI studies have suggested that cues calling attention to a temporal interval might activate left hemisphere areas (Coull et al., 2000, Coull et al., 2001); (2) orienting would activate a superior parietal region and the temporal parietal junction, with a right hemisphere bias (Corbetta et al., 2000); and (3) conflict would activate anterior cingulate cortex (ACC) and a left lateral frontal bias might be suggested for the importance of dopamine for this system (Bush et al., 2000, MacDonald et al., 2000).

Section snippets

Subjects

Sixteen right-handed normal adults (mean age = 27.2 years, SD = 5.7 years, range: 18–36 years; 8 female) participated in this study. They were scanned in a scanner while they carried out the ANT. A signed informed consent approved by the New York Presbyterian Hospital/Weill Medical College of Cornell University was obtained from each participant prior to the experiment.

Attentional network test (ANT)

A version of the ANT was adapted to optimize the attentional contrasts for the fMRI study. We used three cue conditions (no

Behavioral results

Table 1 shows the mean RTs for each condition of the ANT performed during the scan. Repeated measures ANOVA of RT showed that the main effect of target condition (conflict effect) was significant, F(1,15) = 50.86, P < 0.01. The main effect of cue condition was significant, F(2,30) = 30.81, P < 0.01. The interaction between target condition and cue condition was not significant, F(2,30) = 1.51, ns. The alerting effect was significant, F(1,15) = 49.83, P < 0.01, and the orienting effect was

Discussion

Overall, results support the initial hypotheses that specific attention networks operating within the same subjects and within the same task-blocks are associated with separable activation patterns loading on specific anatomical regions. Several studies have suggested that alerting depends upon the norepinephrine system by showing that the effect of warning signals is reduced or eliminated by norepinephrine antagonists (Coull et al., 1996, Coull et al., 2001, Marrocco and Davidson, 1998). We

Acknowledgments

Supported by NSF grant BCS 9907831 and by a DeWitt Wallace-Reader's Digest Research Fellowship in Psychiatry. The authors would like to thank Drs. Yihong Yang, Hong Gu, Michael Worden, and Amir Raz for their help.

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