Micro- and Macro-Psychological Analyses of Attention and the Role of Cholinergic Systems

Abstract

Attention is critical for interacting with our dynamic cue-rich environments and consequently attentional deficits can escalate to yield incapacitating disorders. In order to develop rational treatments for the attentional instabilities that typify a wide range of brain disorders, it is crucial that we determine the validity of behavioral tasks used to reveal neurobehavioral and neurocognitive mechanisms of attention in both rodent models and healthy and impaired humans. Measures of behavioral performance from tasks with little or uncertain validity yield misleading neuro-behavioral mappings that offer little translational utility. Here, we assessed the construct validity of a common rodent attentional task, the Sustained Attention Task (SAT), examined competing models for the psychological mechanisms which mediate effects of performance challenges thought to tax attentional resources or effort, and determined individual differences in the neurobiological and cognitive mechanisms for SAT performance. Dominant conceptualizations about the psychological nature of the SAT have assumed that it necessitates “top-down”, or goal-directed, attentional control for the successful detection of relatively rare stimuli. The work presented in this dissertation challenges the assumption that in all individuals, SAT engages “top-down” attentional mechanisms. Specifically, animals with relatively “hot” cognitive-motivational styles (sign-trackers), prone to attributing incentive motivational properties to reward predictive cues, engage perceptual, but not cholinergic-attentional mechanisms to respond to salient cues in SAT. Next, we examined the cognitive mechanisms underlying task decline or maintenance in SAT, particularly in the face of challenges. To this aim we tested two competing models of effortful performance: the resource depletion model and the opportunity cost model. The former proposes that performance on tasks, such as the SAT, declines over time as a function of consumed biological and psychological resources. However, this model fails to explain a number of critical features of effortful performance and can be methodologically irrefutable. Alternatively, the opportunity cost model is computationally accessible, proposing that task performance declines as a result of subjective feelings of effort arising from cost/benefit calculations for the value of staying on task versus switching to an alternate action. We employed SAT manipulations proposed to alter the demands on task-related processing resources versus opportunity costs associated with task maintenance in opposing directions. Male and female rats trained to SAT criterion performed four versions of SAT: with a flashing house light distractor (dSAT), dSAT with a rest period from task performance, with blocks where the intertrial interval (ITI) is shortened, and with blocks where the ITI is lengthened. Importantly, the two competing theoretical perspectives predict opposed outcomes of these task manipulations: long ITIs should not tax attentional resources, but they should be neutral to or elevate opportunity costs. Conversely, shorter ITIs are thought to tax processing resources but may be neutral with respect to, or even decrease, opportunity costs. The rest period during dSAT is proposed to offer relief and restoration for consumed resources while remaining neutral to opportunity costs. The results from these manipulations were not consistent with a resource depletion account of task maintenance nor did they conform to predictions set by the opportunity cost model. Collectively, the data presented in this dissertation have established a research program designed to determine the construct validity of SAT, to test competing psychological theories about the mechanisms involved in the response to task manipulations, and further examined individual differences in attentional strategies.