Review
Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis

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Abstract

In traditional accounts, fluctuations in sustained and focused attention and associated attentional lapses during task performance are regarded as the result of failures of top-down and effortful higher order processes. The current paper reviews an alternative hypothesis: that spontaneous patterns of very low frequency (<0.1Hz) coherence within a specific brain network (‘default-mode network’) thought to support a pattern of generalized task-non-specific cognition during rest, can persist or intrude into periods of active task-specific processing, producing periodic fluctuations in attention that compete with goal-directed activity. We review recent studies supporting the existence of the resting state default network, examine the mechanism underpinning it, describe the consequent temporally distinctive effects on cognition and behaviour of default-mode interference into active processing periods, and suggest some factors that might predispose to it. Finally, we explore the putative role of default-mode interference as a cause of performance variability in attention deficit/hyperactivity disorder.

Introduction

The capacity to effectively establish and actively maintain a sustained focus of mental activity during goal-directed tasks is both a necessary aspect of successful information processing (Van der Linden et al., 2005) and a key element of human productivity in post-industrial economies (Lanham, 2006). This is underlined by the fact that deficits in sustained/focused attention are an inherent feature of a number of debilitating psychiatric conditions (Brooks et al., 2006; Liu et al., 2002; Swaab-Barneveld et al., 2000). Neuropsychological models of deficient focused and sustained attention implicate both trait-like deficits, such as those seen in individuals with psychiatric conditions, and state-related variations associated with fatigue or fluctuations in arousal and alertness, as causes of sustained attention deficits (Ballard, 1996, Denney et al., 2005). The traditional view is that fluctuations in the quality of sustained attention occur when these trait and state factors act alone or together to limit the resources available for the top-down and effortful control of attention in a way that reduces attentional focus and increases susceptibility to both intrinsic and extrinsic distractions as time passes (Silver and Feldman, 2005).

The mechanisms that are presumed to account for such deficiencies in top-down control have remained unspecified. In this paper we review a proposed mechanism which is emerging in the neuroscience literature. The hypothesis is that fluctuations in the quality of sustained and effortful attention occur, at least in part, because of a failure to fully and effectively transition from a baseline ‘default-mode’ to an active processing mode during performance of cognitive tasks. This leads to a situation in which activity characteristic of resting brain states, associated with a pattern of task-independent generalized cognition, has the potential to interfere with and reduce the effectiveness of active cognitive processes required for goal-directed task performance. This hypothesis emerges from the recent observations that distributed neural circuits demonstrate coherent low frequency (<0.1Hz) fluctuations. One such network, termed the ‘default-mode’ network is particularly observable during resting states, and its activation is conjectured to be incompatible with goal-directed activity (Fox et al., 2005). This hypothesis predicts that disturbances in attention due to interference by the default mode would produce a distinctive pattern of slowly fluctuating attention with episodic lapses and a pattern of periodic and transitory performance deficits (e.g., manifest as increases in reaction time and increased frequency of errors). There are four sections in the current paper. First, the concept of the default-mode network is introduced, its functional neuroanatomy described, its synchronization through low frequency neuronal oscillations (<0.1Hz) highlighted, and the cognitive processes thought to be subserved by it are reviewed. Second, the case that default mode related cognitions can interfere with task-related performance is set out, and the default-mode interference hypothesis is delineated. Third, a possible framework for thinking about individual and task-related factors that might constrain effective transitioning from rest to goal-directed activity is presented. Finally, the default-mode hypothesis is applied to recent findings of reaction time variability in Attention-Deficit/Hyperactivity Disorder (ADHD) and the suggestion that this corresponds to a low frequency pattern (Castellanos et al., 2005).

Section snippets

Default-mode networks of neuronal activity related to task independent cognition during ‘rest’ are spontaneously synchronized at very low frequencies

Classical models of attentional control give little systematic consideration to the different attentional states that exist in real world settings (Smilek et al., 2006). Historically the focus has been almost exclusively on attention as a platform for active, goal-directed, and focused processing of information (Kingstone et al., 2003). Modes of more diffuse or internally oriented attention associated with other attentional states such as rest, relaxation and introspection have been largely

Default-mode interference: a potential cause of spontaneous attentional fluctuations and periodic attentional lapses during task performance

Taken as whole it can be argued that this pattern of alternation between an introspective and extrospective state, whatever their specific functions, represent a coherent and integrated system of intrinsic activity which subserves important cognitive functions in general. However, at any one particular point in time there is an exclusivity of function between the two attentional orientations sub-served by two components of the default-mode network: simultaneous engagement in either of these

What state-related factors might increase default-mode interference?

The extent to which default-mode interference occurs and then proceeds to interrupt goal-directed task performance depends on the extent to which a successful transition from rest to active processing can occur. Fig. 4 provides a pictorial representation of the factors that might affect this process of transition and therefore increase or reduce the probability of default-mode interference occurring. Four elements are considered; affinity to the default mode, affinity to goal-directed state

Reflections on the default-mode interference hypothesis and attention variability in ADHD

State-related variables such as those described above will inevitably interact with trait-type features in determining the liability to default-mode interference. In terms of the model described these will manifest as intrinsic differences in resting state affinity, task affinity, sensitivity to extrinsic motivation and effort-related resources. Individuals differ in their tolerance for boredom and the extent to which they are intrinsically motivated by a particular task. Given the significance

Summary

In the current paper we have set out a hypothesis to explain the existence of spontaneous fluctuations in attention in relation to recent findings of low frequency coherence across default-mode brain networks during rest and their potential to persist into and interfere with periods of active processing. What is required now is a systematic approach exploring the default mode and associated cognitive activity during periods of transition from rest to active processing under different conditions

Acknowledgments

The authors are indebted to a number of colleagues for their valuable contribution to initial discussions of the ideas presented in this paper. In particular we would like to thank Michael Milham, Daniel Margulies, Bharat Biswal, Mitul Mehta, Adriana Di Martino, Judith Walters, Susannah Helps and other members of the ADHD Neuroscience Network (ANNet). We would also like to thank Marcus Raichle and Michael Fox for their kind permission for the use of Fig. 1.

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