ReviewThe cognitive neuroscience of sustained attention: where top-down meets bottom-up
Introduction
Beginning with Mackworth’s experiments in the 1950s, the assessment of sustained attention (or vigilance) performance typically has utilized situations in which an observer is required to keep watch for inconspicuous signals over prolonged periods of time. The state of readiness to respond to rarely and unpredictably occurring signals is characterized by an overall ability to detect signals (termed ‘vigilance level’) and, importantly, a decrement in performance over time (termed ‘vigilance decrement’). The psychological construct of ‘vigilance’, or ‘sustained attention’, has been greatly advanced in recent decades, allowing the development and validation of diverse tasks for the test of sustained attention in humans and animals and thereby fostering research on the neuronal circuits mediating sustained attention performance in humans and laboratory animals.
Sustained attention represents a basic attentional function that determines the efficacy of the ‘higher’ aspects of attention (selective attention, divided attention) and of cognitive capacity in general. Although impairments in the ability to detect and select relevant stimuli or associations are intuitively understood to impact modern living skills (e.g., driving a car), cognitive abilities (e.g., acquiring novel operating contingencies of teller machines, or detecting social cues important to communicate effectively), and possibly even consciousness [74], psychological research on sustained attention has largely focused on parametric, construct-specific issues and only rarely addressed the essential significance of sustained attention for higher cognitive functions like learning and memory [17]. In fact, the evidence in support of the fundamental importance of sustained attention for general cognitive abilities has largely been derived from studies in neuropsychiatric populations (see below). Thus, determining the brain networks mediating sustained attention not only represents a crucial step toward understanding the neuronal mechanisms underlying this critical cognitive function, but also toward the development of cognitive neuroscience-inspired theories of neuropsychiatric disorders characterized by impairments in fundamental attentional functions (see below).
Cognitive neuroscience research has consistently documented activation in right hemispheric prefrontal and parietal regions during sustained attention performance. The recent overview by Cabeza and Nyberg [8] illustrates the sobering degree to which such imaging data remain isolated if they are not embedded in a theory describing the neuronal mediation of the cognitive performance of interest. As we have argued earlier [85], the development of such a theory requires converging evidence from studies manipulating the cognitive function of interest (i.e., sustained attention) and measuring brain correlates (typically human imaging studies) with results from experiments on the consequences of manipulations in the integrity, excitability, or integrative capacity of defined neuronal circuits on the cognitive function of interest (typically animal behavioral–neuroscientific studies). Such converging evidence ensures that research aimed at explaining complex high-level cognitive functions by successively lower neural levels of description benefits from neuroscientific research approaches, and that efforts to determine low-level neuronal mechanisms of cognitive functions benefit from cognitive construct-driven research in humans [25], [63], [76]. Furthermore, it is crucial that evidence in support of neuronal circuits acting top-down to modulate attentional information processing (e.g., Ref. [75]) will be integrated with evidence on the role of ascending cortical input systems to arrive at a comprehensive theory of sustained (or any other form of) attention. In other words, the title phrase ‘where-top down meets bottom-up’ reflects two interrelated issues, that is (1) the convergence of information generated by cognitive-neuroscience research in humans and by the more fundamental neurosciences that is required to attribute sustained attention to defined neuronal circuits [85], and (2) the convergence of the functions mediated via top-down cognitive processes and bottom-up sensory input processing that is crucial for sustained attentional performance. These convergences are the focus of this review, indicating that the different levels of analysis employed by cognitive neuroscience research on sustained attention have sufficiently developed, albeit largely separately, to permit now an integration of evidence and therefore the development of a theory about the neuronal mediation of sustained attention.
The terms ‘top-down’ and ‘bottom-up’ processes, and the special focus of this review, require further clarification. ‘Top-down’ or ‘bottom-up’ regulation of attentional processes represent conceptual principles rather than referring to anatomical systems, such as ascending and descending projections. ‘Top-down’ processes describe knowledge-driven mechanisms designed to enhance the neuronal processing of relevant sensory input, to facilitate the discrimination between signal and ‘noise’ or distractors, and to bias the subject toward particular locations in which signals may appear [41]. For example, in sustained attention performance, the subject knows where to expect what type or modality of signal, how to respond in accordance with previously acquired response rules, and so forth. Furthermore, the subject develops expectations concerning the probability for signals and strategies for reporting signals versus false alarms (see below). All these variables influence performance, based on mechanisms that range from changes in sensory signal processing to the enhanced filtering of distractors and the modification of decisional criteria.
Such a ‘top-down’ biasing of attentional performance contrasts with ‘bottom-up’ perspectives that describe attentional functions as driven mainly by the characteristics of the target stimulus and its sensory context [97]. ‘Bottom-up’ perspectives attempt to explain a subject’s ability to detect targets and target-triggered attentional processing largely by the sensory salience of the targets, and their ability to trigger attentional processing by recruiting ‘higher’ cortical areas in a bottom-up manner (e.g., from the processing of a visual target in the primary visual cortex to temporal regions for object identification and to parietal regions for location). Importantly, ‘top-down’ and ‘bottom-up’ processes represent overlapping organizational principles rather than dichotomous constructs, and in most situations, top-down and bottom-up processes interact to optimize attentional performance [22].
Activation of top-down processes are traditionally considered a component of the frontal cortical mediation of executive functions. Such processes were previously conceptualized in the context of attention by Posner and Petersen’s [75] anterior and posterior attention systems that function to detect targets and bias the subjects’ orientation to target sources, respectively. Data from human imaging and primate single unit recording studies have substantiated the notion of top-down processes by demonstrating sequential activation of frontal-parietal–sensory regions, including decreases in activity in task-irrelevant sensory regions, and the modulation of neuronal activity in sensory and sensory-associational areas reflecting the top-down functions described above [19], [39], [41], [93]. This review focuses on the functions of the basal forebrain cholinergic projections to the cortex as a major component of the activation of top-down processes in the mediation of sustained attention. To avoid confusion, it should be reiterated that therefore, the anatomically ascending basal forebrain system is proposed to contribute to the functionally top-down processes in sustained attention.
As will be discussed below, the activation of cortical cholinergic inputs as a major component of the top-down processes in sustained attention performance acts to bias the processing of sensory inputs at all levels of cortical sensory information processing, thereby facilitating and maintaining sustained attention performance. Fig. 1 captures this hypothesis by illustrating the anterior attention system and its top-down regulation of posterior and sensory cortical information processing ( [75]; see also legend for Fig. 1). The basal forebrain cholinergic corticopetal projection system is conceptualized as a major and necessary component of these top-down processes. In sustained attention, this projection system is activated, via direct connections from the prefrontal cortex to the basal forebrain. Increased activity in cortical cholinergic inputs, that terminate in all cortical regions and layers, facilitate all aspects of the top-down regulation of sustained attention performance, ranging from the enhanced sensory processing of targets to the filtering of distractors and the optimization of decisional strategies. Evidence in support of this hypothesis will be discussed in detail, following a description of the construct ‘sustained attention’.
Section snippets
‘Sustained attention’ and ‘arousal’: conceptual overlaps and differences
As the terms ‘vigilance/sustained attention’ and ‘arousal’ have been used interchangeably, particularly in clinical contexts and in interpreting electroencephalographic (EEG) data, the specific meaning of vigilance/sustained attention needs to be defined and dissociated from the more global classification of brain states that include ‘arousal’. Obviously, the ability to perform monitoring tasks requires an activated forebrain and thus depends on ‘arousal’. Likewise, the ‘arousing’ consequences
General interpretational issues
Macroanatomical correlates of sustained attention performance have been determined mainly by two lines of research. First, findings from neuropsychological studies have identified areas of brain damage or degeneration which are correlated with impairments in sustained attention performance. Second, and more recently, functional imaging studies have located areas in the intact brain in which changes in metabolic activity correlate with sustained attention performance.
Complexities in the
Neuronal circuits mediating sustained attention performance
Evidence from studies designed to manipulate the functioning of defined neuronal circuits and assess the consequences for attentional performance, or to record from neurons constituting such circuits in animals performing in attentional tasks, is expected to explain the prominent role attributed to frontal cortical and parietal regions in human neuropsychological and functional imaging studies. Such reductionist explanations are also expected to specify the nature of the processing mediated via
Ascending noradrenergic projections: the ‘arousal’ link?
The basis for the conceptual dissociation between sustained attention and arousal is stressed above. In support of this dissociation, the findings from functional neuroimaging studies have suggested that the neuronal circuits mediating the necessary arousal for proper sustained attention performance differ from those correlated with sustained attention. Specifically, the arousal components may be mediated via activation of the thalamus. Attentional performance-associated increases in thalamic
Relationships with other forms of attention
Given the close theoretical relationships between different aspects of attention (sustained, selective, divided), it should not come as a surprise that the available data from neuropsychological, functional imaging, and animal experimental studies already suggest extensive overlaps in the circuits mediating different aspects of attention (e.g., Refs. [1], [6], [8], [10], [13], [42], [59], [99], [101]). For research purposes, it is important to maintain clear definitions of the aspects of
Major unresolved issues
The hypotheses that the activation of the fronto-parietal areas observed in humans performing sustained attention tasks reflects in part the consequences of cholinergic stimulation of these regions is attractive but remains unsubstantiated. The present model predicts more widespread areas of cortical activation than reported in most of the available studies, although the relatively selective activity changes reported in those studies may in part be due to the methods used to isolate regions of
Conclusions
Sustained attention represents a fundamental component of the cognitive capacities of humans. Aberrations in the ability to monitor significant sources of information rapidly develop into major cognitive impairments. Human neuropsychological and functional imaging studies have pointed to fronto-parietal areas, particularly in the right hemisphere, as being prominently involved in the mediation of sustained attention, or vigilance. Animal experimental evidence strongly supports the basal
Acknowledgements
The authors’ research was supported by NIH grants NS32938, MH57436, NS37026, and AG10173.
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