More attention must be paid: The neurobiology of attentional effort

Abstract

Increases in attentional effort are defined as the motivated activation of attentional systems in response to detrimental challenges on attentional performance, such as the presentation of distractors, prolonged time-on-task, changing target stimulus characteristics and stimulus presentation parameters, circadian phase shifts, stress or sickness. Increases in attentional effort are motivated by the expected performance outcome; in the absence of such motivation, attentional performance continues to decline or may cease altogether. The beneficial effects of increased attentional effort are due in part to the activation of top-down mechanisms that act to optimize input detection and processing, thereby stabilizing or recovering attentional performance in response to challenges. Following a description of the psychological construct “attentional effort”, evidence is reviewed indicating that increases in the activity of cortical cholinergic inputs represent a major component of the neuronal circuitry mediating increases in attentional effort. A neuronal model describes how error detection and reward loss, indicating declining performance, are integrated with motivational mechanisms on the basis of neuronal circuits between prefrontal/anterior cingulate and mesolimbic regions. The cortical cholinergic input system is activated by projections of mesolimbic structures to the basal forebrain cholinergic system. In prefrontal regions, increases in cholinergic activity are hypothesized to contribute to the activation of the anterior attention system and associated executive functions, particularly the top-down optimization of input processing in sensory regions. Moreover, and influenced in part by prefrontal projections to the basal forebrain, increases in cholinergic activity in sensory and other posterior cortical regions contribute directly to the modification of receptive field properties or the suppression of contextual information and, therefore, to the mediation of top-down effects. The definition of attentional effort as a cognitive incentive, and the description of a neuronal circuitry model that integrates brain systems involved in performance monitoring, the processing of incentives, activation of attention systems and modulation of input functions, suggest that ‘attentional effort’ represents a viable construct for cognitive neuroscience research.

Introduction

Increasing attentional ‘effort’ as a result of challenging circumstances, and as a function of the motivation to maintain or recover attentional performance, represents an everyday experience. To paraphrase and modify a famous statement: every one knows what increases in attentional effort are. For example, consider your drive home from work; yesterday it was uneventful and you used a well-practiced route that makes minimal demands on your attentional resources; indeed, you do not even recall whether the traffic light actually was on green as you made it through that intersection. But today, you did not sleep much last night, you had an exhausting day, or you feel that you are getting sick, and you are having trouble concentrating, but the last thing you need is another ticket. You will increase your attentional ‘effort’ to ensure that you will not miss a red light or a sign, and you will also closely monitor your speed, while looking out for that police car.

However, theoretically and experimentally, ‘attentional effort’ has remained an undefined concept. Indeed, James (1890) dismissed the issue outright, concluding that “… the notion that our effort in attending is an original faculty, a force additional to the others of which brain and mind are the seat, may be an abject superstition” (p. 452). “Attentional effort” typically has been cited in the literature in order to explain the performance in difficult tasks, or in tasks involving attentional shifts or switching modalities. Thus, ‘attentional effort’ has been generally considered a function of task difficulty. An arguably more useful conceptualization of attentional effort, as a function of the subject's motivation to perform, particularly following performance challenges, is proposed below. Furthermore, we present a model that describes the interactions between cortical, mesolimbic and cholinergic systems considered essential for activating attentional systems and resources as a result of performance challenges and the subjects' motivation to recover performance or limit performance decline. This model also provides avenues toward the dissociation between attentional processes and changes in reward contingencies (Maunsell, 2004).