Selective Attention, Working Memory, and Executive Function as Potential Independent Sources of Cognitive Dysfunction in Schizophrenia

James M. Gold; Benjamin Robinson; Carly J. Leonard; Britta Hahn; Shuo Chen; Robert P. McMahon; Steven J. Luck

Disclosures

Schizophr Bull. 2018;44(6):1227-1234. 

In This Article

Abstract and Introduction

Abstract

People with schizophrenia demonstrate impairments in selective attention, working memory, and executive function. Given the overlap in these constructs, it is unclear if these represent distinct impairments or different manifestations of one higher-order impairment. To examine this question, we administered tasks from the basic cognitive neuroscience literature to measure visual selective attention, working memory capacity, and executive function in 126 people with schizophrenia and 122 healthy volunteers. Patients demonstrated deficits on all tasks with the exception of selective attention guided by strong bottom-up inputs. Although the measures of top-down control of selective attention, working memory, and executive function were all intercorrelated, several sources of evidence indicate that working memory and executive function are separate sources of variance. Specifically, both working memory and executive function independently contributed to the discrimination of group status and independently accounted for variance in overall general cognitive ability as assessed by the MATRICS battery. These two cognitive functions appear to be separable features of the cognitive impairments observed in schizophrenia.

Introduction

Impairments of attention, working memory, and executive control are central features of the cognitive deficits observed in people with schizophrenia (PSZ) and all are plausibly implicated in the broad neuropsychological impairment observed in schizophrenia.[1] However, there is substantial overlap in how these terms are used in the literature, and it remains unclear if these represent distinct deficits or differing manifestations of a single underlying deficit in the ability to use internal representations to guide behavior. Although abstract, this question has practical implications for targeting interventions designed to improve cognition.

Some initial distinctions can be established. Working memory (WM) involves the brief maintenance of information in the service of ongoing behavior.[2] Two aspects of WM can be separated: (1) the capacity of WM, how much information can be stored, and (2) the ability to manipulate the stored information. In this article, we focus on WM capacity, not manipulation. Attention—specifically selective attention—involves operations that prioritize the processing of a subset of available inputs while suppressing the processing of other inputs.[3] Such priority may arise because some stimuli are task-relevant (often called top-down control), or because some stimuli are so salient that they attract attention relatively automatically (often called bottom-up control,[4]). For this study, we are focusing on only one of the many components of executive function, the ability to maintain and flexibly update the "rules" that apply to the current sets of stimuli and response alternatives.[3,5,6] Successful updating necessarily involves inhibition of prior rules so that behavior is guided by the current rule.

While these definitions imply separable systems, the operation of these processes is interactive. For example, the efficient use of WM requires the use of selective attention so that storage capacity is devoted to task-relevant information.[7] Similarly, the operation of selective attention requires the maintenance of a search template/rule that biases perceptual systems so that task-relevant representations gain a competitive advantage over irrelevant representations for further processing.[8] The case becomes more complicated with executive control. Executive control requires active maintenance of rules to bias perceptual processing/response selection and the ability to update rules in the face of changing circumstances. Executive control is realized through an integration of selective attention and WM in the service of behavioral goals. Thus, these processes are interactive, and impairments in one will impact the other. However, this does not mean that there are no practical distinctions among attention, WM, and executive control. By analogy, the heart, lungs, and vasculature are densely interactive and yet are clearly separable.

The goal of this article is to examine the relationship between these constructs and how they relate to diagnostic status and general cognitive ability as assessed by the MATRICS battery which is widely used to characterize cognitive function in PSZ.[9] To assess selective attention, we used a visual search paradigm where PSZ have difficulty using top-down control to guide search, whereas bottom-up control of search is intact.[10] Importantly, the search task imposed minimal WM or executive control demands because as the search target remained constant across trials. To assess WM, we used a variant of visual change detection (called change localization), where PSZ show marked capacity deficits that are highly correlated with broad cognitive performance.[11,12] The WM displays did not include any distractors, minimizing the need for selective attention, and the task rules remained constant over trials, minimizing demands on executive control.

To measure executive function, we used a variant of the AX CPT called the 1–2 AX CPT.[13] In this task, participants see a context cue (either a 1 or a 2) followed by a series of letters. The context cue "1" indicates that an X following, an A is the target whereas a context cue of "2" indicates that a Y following a B is the target for that series. This task puts a premium on the ability to maintain and update rules: the same letter sequence is a target following one context cue and a distractor following the alternative context cue, and this sequence must be maintained to guide a series of target vs nontarget decisions. How are the WM demands different in change localization vs the 1–2 AX CPT? Change localization provides an estimate of how much information a person is capable of storing in WM. In the 1–2 AX CPT, the demand is to dynamically update and maintain rules to guide the use of WM itself: the context cue must be maintained and applied to additional items (ie, the A cue), which must then be maintained in order to respond to the letter (an X or a Y). Thus, although 1–2 AX CPT requires WM, it stresses updating processes, whereas change localization stresses storage capacity.

Even using these refined measures, we expected all three tasks to be modestly intercorrelated in both groups, because it is virtually impossible to design tasks that are fully process-pure and the three cognitive functions studied here are likely involved in most, if not all, intentional behavior. However, we expected that some measures would cluster together more strongly and that some tasks would be more sensitive to diagnostic group. First, because the visual search task was designed to be independent of updating and WM storage, we expected that visual search performance would be weakly related to change localization and the 1–2 AX CPT. Second, because the 1–2 AX CPT task does require WM storage, we expected that performance of this task would be modestly correlated with change localization. However, because the 1–2 AX CPT involves additional updating operations, we expected that these two tasks would exhibit independence in discriminating diagnosis. We did not expect visual search performance to contribute to group discrimination as we previously observed larger between group effects for WM capacity than for top-down visual search slope.[9,10]

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