Elsevier

Brain and Cognition

Volume 70, Issue 2, July 2009, Pages 209-220
Brain and Cognition

Testing the behavioral interaction and integration of attentional networks

https://doi.org/10.1016/j.bandc.2009.02.002Get rights and content

Abstract

One current conceptualization of attention subdivides it into functions of alerting, orienting, and executive control. Alerting describes the function of tonically maintaining the alert state and phasically responding to a warning signal. Automatic and voluntary orienting are involved in the selection of information among multiple sensory inputs. Executive control describes a set of more complex operations that include detecting and resolving conflicts in order to control thoughts or behaviors. Converging evidence supports this theory of attention by showing that each function appears to be subserved by anatomically distinct networks in the brain and differentially innervated by various neuromodulatory systems. Although much research has been dedicated to understanding the functional separation of these networks in both healthy and disease states, the interaction and integration among these networks still remain unclear. In this study, we aimed to characterize possible behavioral interaction and integration in healthy adult volunteers using a revised attention network test (ANT-R) with cue-target interval and cue validity manipulations. We found that whereas alerting improves overall response speed, it exerts negative influence on executive control under certain conditions. A valid orienting cue enhances but an invalid cue diminishes the ability of executive control to overcome conflict. The results support the hypothesis of functional integration and interaction of these brain networks.

Introduction

One of the most important goals of cognitive neuroscience is in understanding of the sources of voluntary control of thoughts, feelings, and actions. One view of attention refers to it as the activity of a set of brain networks that influence the priority of computations of other brain networks for access to consciousness and observable behavior (Posner and Fan, 2008, Raz and Buhle, 2006). According to this description, attention serves as the basis of various control systems. This view conceptualizes the attentional system in specific functional and anatomical terms as comprising three separable functional components of alerting, orienting, and executive control (Posner and Fan, 2008, Posner and Petersen, 1990).

Alerting provides the capacity to increase vigilance to an impending stimulus. While tonic or intrinsic alertness is defined as wakefulness and arousal, phasic alertness represents the ability to increase response readiness to a target subsequent to an external warning stimulus. Alerting involves a change in the internal state in preparation for perceiving a stimulus. For example, following presentation of a warning signal, there are a variety of changes in heart rate and brain oscillatory activity that serve to inhibit competing activities (Kahneman, 1973). The alert state is critical for optimal performance in tasks involving higher cognitive functions (Fan, Raz, & Posner, 2003). Alerting function has been associated with thalamic, frontal, and parietal regions, and is influenced by the cortical distribution of the brain’s norepinephrine (NE) system that arises from the midbrain nucleus locus coeruleus (LC) (Coull et al., 1996, Marrocco et al., 1994).

The orienting function involves aspects of attention that support the selection of specific information from numerous sensory inputs. Orienting can be reflexive (exogenous), as when a sudden target event draws attention to its location; or it can be voluntary (endogenous), as when a person searches the visual field looking for a target. Overt orienting is often associated with head and/or eye movements toward the target; however, it is also possible to enhance target processing by orienting attention covertly, that is, without a change in posture or eye position. Orienting involves rapid or slow shifting of attention among objects within a modality or among various sensory modalities, with three elementary operations: disengaging attention from its current focus, moving attention to the new target or modality, and engaging attention at the new target or modality (Posner, Walker, Friedrich, & Rafal, 1984). In behavioral studies, orienting is often manipulated by presenting a cue indicating where a subsequent target will (or will not) appear (Posner, 1980). A valid cue indicates the location in which an impending target will appear. If the cue is invalid, the target appears in a different location, often opposite to the location indicated by the cue. The benefit in terms of target processing efficiency conferred by valid cues is less in magnitude than the cost associated with orienting to an incorrect location. The orienting system for visual events has been associated with such brain areas as the superior and inferior parietal lobule, frontal eye fields (FEF), and subcortical areas such as the superior colliculus of midbrain and the pulvinar and reticular nuclei of the thalamus (Corbetta et al., 2000, Corbetta and Shulman, 2002, Posner, 1980, Posner and Cohen, 1984, Posner et al., 1982). These areas are thought to carry out different elementary operations involved in the act of orienting. Cholinergic systems arising in the basal forebrain play an important role in modulating orienting.

The executive control function of attention involves more complex mental operations in detecting and resolving conflict between computations occurring in different brain areas (Botvinick et al., 2001, Bush et al., 2000). A number of studies have examined executive control under this framework by using variants of the color Stroop task that require people to respond to one dimension of a stimulus rather than another stronger, but conflicting, dimension (Botvinick et al., 2001, Bush et al., 2000, Fan, Flombaum, et al., 2003, Liu et al., 2004, MacDonald et al., 2000). Other tasks involving cognitive conflict, such as variants of the flanker task developed by Eriksen and Eriksen (Eriksen & Eriksen, 1974), have also been used to evaluate the efficiency of executive control (Botvinick et al., 1999, Casey et al., 2000, Fan, Flombaum, et al., 2003). In everyday life, executive control is most needed in situations that involve planning or decision-making, error detection, novel or not well-learned responses, conditions judged difficult or dangerous, and in overcoming habitual actions. Executive control of attention has been associated with the anterior cingulate cortex (ACC) and lateral prefrontal cortex (Matsumoto & Tanaka, 2004), which are target areas of the ventral tegmental dopamine system (Benes, 2000).

Alerting, orienting, and executive control have been thought to be relatively independent aspects of attention with each subserved by separable brain networks. In the original report of our work with the Attention Network Test (ANT) (Fan, McCandliss, Sommer, Raz, & Posner, 2002) (see Fig. 1 of this ref.), we found that there was a good deal of support for independence across networks. This was shown by the lack of correlation between the performance scores obtained for each network. We conducted an event-related fMRI study to explore the brain activity of the three attention networks (Fan, McCandliss, Fossella, Flombaum, & Posner, 2005). We found the expected brain areas unique to each network. However, we also found substantial areas of overlap. Our most recent finding of distinctive time-frequency patterns associated with each attentional function (Fan, Byrne, et al., 2007) provides further support for the separation of attention into distinct functional networks and suggests that these attentional networks are associated with network-specific oscillation patterns and time courses.

Although the original configuration of the ANT demonstrated independence of the networks, it would be surprising if the networks did not subserve attentional functions through coordinated activity. The networks should interact in the performance of many acts of attention. Evidence of interaction appeared even in our early studies. For the behavioral performance, where there were two small but significant interactions in which the alerting cue (including the center cue and double-cues, in which the cues are displayed at two possible locations but provide only temporal information and not spatial information) conditions, compared to no-cue and orienting cue (spatial-cue, in which the cue predicts the location of the target and provides both temporal and spatial information) conditions, the efficiency of the executive control network for target response was reduced (Fan et al., 2002). In a study with a larger sample using the ANT, we found a small but significant negative correlation between the alerting and executive control scores (Fossella et al., 2002). In studies using a tone for the auditory alerting signal, alerting inhibits executive control and orienting enhances executive control (Callejas et al., 2005, Callejas et al., 2004), while alerting has been shown to enhance orienting (Fuentes & Campoy, 2008). We have shown that alerting modulates the overall activity of the executive control network, and that orienting interacts with executive control (Fan, Byrne, et al., 2007). For the brain response, we have observed that the ACC is involved in both response anticipation (alerting) and response conflict (executive control) (Fan, Kolster, et al., 2007).

This body of evidence leads us to hypothesize that there exist subtle yet significant interactions and integrations among attentional networks that some previous studies have failed to detect. Such interactions, if found, would shed important new light on how anatomically distinctive attentional networks in the brain work together to support the function of attention. Our strategy to find such interactions is to design tasks in which possible but subtle interactions among attentional networks can be magnified via manipulations so that their effects can be detected at the behavioral level.

One important attentional network that may contribute to such interactions and integrations might be the orienting network. However, the original ANT did not incorporate invalid cues. Therefore, the interaction between orienting and executive functions could not be explicitly examined. In this study, we manipulated the validity of the cue. We know from previous work that using partial validity would allow one to compare valid and invalid trials and get a much more specific measure of the shift of orientation from an expected to an unexpected location. This manipulation enabled us not only to test the validity effect and its interaction with conflict processing, but also to measure the elementary operations of orienting. We predicted that the invalid cues with low probability may demand more attentional resources than the valid cues with high probability. Therefore, the former may have negative impact on the conflict processing by the executive control network.

The second important interaction lies between the alerting and executive control networks. This is related to the finding that alerting and executive control share some common brain structures. In this study, we manipulated the cue-target interval so that the interaction between alerting and conflict processing can be examined. We predicted that, although alerting improves overall RT, there would be a negative impact of alerting on executive control under a certain cue-target interval because of overlap of attentional processes involving shared resources. In addition, for target processing, the flanker and location conflicts were manipulated so that we were able to examine dual-conflict processing. It should be noted that only the conflict processing function of the executive control network was tested in this study. Uncovering the patterns in which these networks interact with each other will shed new light on understanding how attention works as a whole.

Section snippets

Participants

Thirty young adult volunteers (15 females and 15 males; mean age, 25.4 years; range, 22–34 years) participated in this study. The consent procedure was approved by the institutional review board and written informed consent was obtained from each participant.

The revised attention network test (ANT-R)

We designed the ANT-R based on the original ANT (Fan et al., 2002) in order to optimize the attentional contrasts and to examine the interaction between attentional networks. The revised version uses three, instead of four, cue conditions

Results

Table 1, Table 2 show the RT and accuracy (mean and SD) under all the conditions. The overall RT was 604 ms (SD = 59 ms) and the overall accuracy of the task performance was 94% (SD = 4%).

Discussion

The most intriguing finding of the current study is that alerting improves overall response speed while it exerts negative influence on executive control under certain conditions. The small but negative alerting by flanker congruency interaction is consistent with what we found previously. Although the alerting cue conditions improved overall RT compared to no-cue conditions, the conflict effect was greater under the alerting cue, especially under the 400 ms cue-target interval condition. We

Acknowledgments

This work was supported by a NARSAD Young Investigator Award and by a NIMH grant MH083164 to JF.

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