Alterations of the attentional networks in patients with anxiety disorders

Abstract

Cognitive theories of emotion try to explain how anxious people attend to the world. Despite the increase in empirical research in this field, the specific or general attentional impairments of patients with anxiety disorder is not well defined. We decided to investigate the relationship between pathological anxiety and attentional mechanisms from the broader perspective of the attentional networks. In our study, patients with anxiety disorders and control participants carried out a task to assess efficiency of three attentional networks: orienting, alerting, and executive control. The main result was that anxiety disorders are related to both reduced effectiveness of the executive control network and difficulties in disengaging attention from invalid cues, even when using emotionally neutral information. This relationship between these attentional networks and anxiety may in part explain the problems in the day-to-day functioning of these patients.

Introduction

Our knowledge and understanding of emotions have advanced considerably over the last 30 years. During this time, it has become clear that emotions have an adaptive function and they are closely related to cognitive processes (see Dolan, 2002, Pessoa, 2008, for reviews). Usefulness of emotional regulation in maintaining that adaptive role has also been highlighted (Ochsner & Gross, 2008). When a person has problems in controlling emotions under specific circumstances, failing to select the most adaptive option, this can lead to a heterogeneous group of affective disorders such as bipolar affective disorder, depression, or anxiety disorders (DSM-IV-TR, 2000).

Increased prevalence of these disorders and the impairment of quality of life associated with them in both physical and social fields (Barrera & Norton, 2009), has caused a growing interest in therapeutic intervention over the past 25 years (Boschen, 2008). Many efforts have been made in developing adequate therapies and theories highlighting the factors that make us vulnerable to the above-mentioned disorders. Trait-anxiety, disgust sensitivity (McDonald, Hartman, & Vrana, 2008), the Looming Cognitive Style (Riskind, Black, & Shahar, 2010), or experiential avoidance (Berman, Wheaton, McGrath, & Abramowitz, 2010) have been considered among these factors, most of which are closely related to attentional or regulatory processes.

Empirical research in this field has demonstrated that basic processes of regulation (i.e., attentional deployment, reappraisal, or suppression) rely on the efficiency of the attentional system, thus showing a relationship between attention, regulation deficits and anxiety disorders (Amstadter, 2008, Gross, 1999). Given the important relationship between attention and anxiety (Yiend, 2010), a large body of information-processing biases has been considered by cognitive theories of anxiety explaining how anxious people attend to the world. Specifically, most theories are based on the distinctive sensitivity to threat-related stimuli shown by anxious individuals, leading to a great amount of research using different attentional tasks (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van IJzendoorn, 2007).

In general, anxiety is related to hypervigilance and to both facilitation and interference, depending on the procedure that is used to investigate attentional biases. If the negative stimuli are the target to be detected, anxious participants show better performance (Fox et al., 2001, Öhman and Mineka, 2001, Öhman et al., 2001), but when negative stimuli are distracters, performance of anxious participants is consequently impaired due to increased distractibility (Derryberry and Reed, 2002, Fenske and Eastwood, 2003). Although these assumptions are well established, effects of the different types of anxiety (state and trait) on these processes are not yet clear. Some findings have led researchers to propose an interaction between trait and state factors or the necessity of both (Broadbent & Broadbent, 1988). Other findings assign the same relevance to results obtained under state and trait-anxiety (Fox et al., 2001). Other authors suggest that trait-anxiety would give rise to a bias to constantly direct attention towards the source of threat, state-anxiety only increasing that threat value (Williams, Watts, MacLeod, & Mathews, 1988).

For more than a century, attention was identified by cognitive science as a unitary system. However, it is currently conceived as a group of systems or networks. Corbetta (1998, p. 831) defines attention as “the mental ability to select stimuli, responses, memories, or thoughts that are behaviorally relevant, among the many others that are behaviorally irrelevant.” That selection process is based on two complementary and different processing systems (top-down and bottom-up). Other authors (Posner & Petersen, 1990) have proposed three specific functionally and anatomically distinct attentional networks: alerting, orienting and executive control (see Posner, Rueda, & Kanske, 2007, for a review). Therefore, it is important to understand the relationships between the different types of anxiety (state, trait, and clinical) in this broader framework of attention.

The characteristic effects of trait vs. state anxiety on the attentional system could perhaps be better understood if we take into account the Corbetta and Schulman's Neuroanatomical Model of Attention (2002). They differentiate between two distinct attentional systems. One is involved in preparing and applying goal-directed (top-down) selection of stimuli and responses, such as attitudes or strategies, possibly related to personality traits. As mentioned above, trait-anxiety gives rise to a bias to constantly direct attention towards the source of threat. The other system (bottom-up) is sensitive to stimuli salience. Given that state anxiety increases the threat-value of stimuli and/or is a consequence of the events occurring in a particular situation, this kind of anxiety should be related to the bottom-up system. Thus, we propose that it can be helpful to consider trait and state anxiety as being related to top-down and bottom-up systems, respectively. This idea is further supported by recent research (Pacheco-Unguetti, Acosta, Callejas, & Lupiáñez, 2010).

On the other hand, following Posner and Rothbart, attention can be considered a system with different functions, each subtended by a different set of brain structures (i.e., different attentional networks), all working with the goal of modulating behaviour in order to better adapt to environmental circumstances (Posner & Rothbart, 2007). Therefore the relationship between different types of anxiety and attention could undoubtedly be better understood if we consider attention from this broader perspective.

Alerting network. This alerting system is involved in establishing a vigilant state and maintaining readiness to react. Two types of alertness have been described. Phasic alertness is related to nonspecific activation as induced by warning cues, and can be measured by comparing responses after a warning cue condition providing temporal information with those in a non-cue condition. Tonic alertness refers to sustained activation over a period of time, and is traditionally measured with vigilance tasks in which participants have to maintain attention for long periods of time in order to detect infrequent stimuli. The Alerting network is implemented on brain areas in the right frontal lobe, right parietal lobe and the locus coeruleus, and is influenced by the norepinephrine system (Marrocco & Davidson, 1998).

Orienting network. Orienting refers to the selection of specific information (location or objects) from numerous sensory inputs. This function can be exerted voluntarily (i.e., endogenous orienting) or reflexively (i.e., exogenous orienting), when a salient stimulus draws attention to its location. Posner proposed three elementary orienting operations: disengaging attention from its current focus, moving to the new location, and engaging at the new target or focus. These operations are supposed to be implemented in the superior and inferior parietal lobe, frontal eye fields, the superior culliculus of midbrain and the pulvinar and reticular nuclei of the thalamus (Posner, Inhoff, Friedrich, & Cohen, 1987). The cholinergic system has an important role in the functioning of this network.

Executive control network. The function of this attentional network is thought to be the detection and resolution of conflicts among thoughts, feelings or responses. Different variants of the Stroop, Flanker or Simon tasks are frequently used to study the efficiency of this attentional network (Eriksen and Eriksen, 1974, Liu et al., 2004). Recent studies have identified activation of the anterior cingulated cortex (ACC) and dorsolateral prefrontal cortex (DLPFC) in cognitive conflict tasks (Fan et al., 2003, Matsumoto and Tanaka, 2004), areas of the mesocortical dopaminergic system.

In this context, Fan, McCandliss, Sommer, Raz, and Posner (2002) developed the Attention Network Test (ANT) to measure the three attentional functions within a single task, combining Posner's cueing paradigm (Posner & Petersen, 1990) with a Flanker task (Eriksen & Eriksen, 1974). Applications of the traditional ANT and its modifications, have demonstrated anatomical independence but cooperation between the three networks (Fan et al., 2002, Fan et al., 2009). Specifically, there are inhibitory relationships between the alerting and executive control network (Posner & Dehaene, 1994), whereas the orienting network raises the efficiency of this last one. The alerting network increases the orienting effect (Callejas, Lupiáñez, & Tudela, 2004).

The attentional networks approach is useful for the exploration of symptoms and pathologies (Berger & Posner, 2000). Specifically the use of ANT and other variants has shown a selective impairment of the executive control network in Alzheimer's Disease (AD; Fernández-Duque & Black, 2006), Borderline Personality Disorder (BPD; Klein, 2003, Posner et al., 2002), Posttraumatic Stress Disorder (PTSD; Leskin & White, 2007), fibromyalgia patients (Miró et al., 2011), and Attention-Deficit Hyperactivity disorder (ADHD; Mullane, Corkum, Klein, McLaughlin, & Lawrence, 2011). Other studies had found alterations of the executive control network together with orienting in squizophrenia (Urbanek et al., 2009, Wang et al., 2005). By contrast, affective disorders such as depression have not revealed any deficit in the functioning of the attentional networks (Murphy and Alexopoulos, 2006, Preiss et al., 2010); although a sadness state has been related to reduced intrinsic alertness (Finucane, Whiteman, & Power, 2010).