Journal of Abnormal Psychology © 2014 American Psychological Association 2014, Vol. 123, No. 4, 783–795 0021-843X/14/$12.00 http://dx.doi.org/10.1037/abn0000003 Hyperfocusing in Schizophrenia: Evidence From Interactions Between Working Memory and Eye Movements Steven J. Luck and Clara McClenon Valerie M. Beck University of California, Davis University of Iowa and University of California, Davis Andrew Hollingworth Carly J. Leonard University of Iowa University of California, Davis Britta Hahn, Benjamin M. Robinson, and James M. Gold University of Maryland School of Medicine Recent research suggests that processing resources are focused more narrowly but more intensely in people with schizophrenia (PSZ) than in healthy control subjects (HCS), possibly reflecting local cortical circuit abnormalities. This hyperfocusing hypothesis leads to the counterintuitive prediction that, al- though PSZ cannot store as much information in working memory as HCS, the working memory representations that are present in PSZ may be more intense than those in HCS. To test this hypothesis, we used a task in which participants make a saccadic eye movement to a peripheral target and avoid a parafoveal nontarget while they are holding a color in working memory. Previous research with this task has shown that the parafoveal nontarget is more distracting when it matches the color being held in working memory. This effect should be enhanced in PSZ if their working memory representations are more intense. Consistent with this prediction, we found that the effect of a match between the distractor color and the memory color was larger in PSZ than in HCS. We also observed evidence that PSZ hyperfocused spatially on the region surrounding the fixation point. These results provide further evidence that some aspects of cognitive dysfunction in schizophrenia may be a result of a narrower and more intense focusing of processing resources. Keywords: schizophrenia, working memory, hyperfocusing, saccadic eye movements, distraction This study tests a recent hypothesis about the nature of impaired intended to explain both attentional abnormalities and reduced attention and working memory (WM) in schizophrenia (Hahn, WM capacity in PSZ. Hollingworth et al., 2012; Hahn, Robinson et al., 2012; Leonard, Although the idea that PSZ have impaired attention is common Kaiser et al., 2013). The essence of this hypothesis is that process- (see review by Luck & Gold, 2008), studies using precise mea- ing resources are focused more intensely1 but more narrowly in sures of selective attention have not found much evidence that PSZ PSZ than in healthy control subjects (HCS). In other words, PSZ have a reduced ability to focus on relevant information and ex- focus unusually strongly on some sources of information to the clude irrelevant information. In the spatial cuing paradigm, for exclusion of others. We call this the hyperfocusing hypothesis. It is example, a cue indicates that attention should be directed to a specific location. Healthy individuals are faster and more accurate when the target is presented at the cued location (valid trials) than when the target is presented at an uncued location (invalid trials) This document is copyrighted by the American Psychological Association or one of its allied publishers. This article was published Online First August 4, 2014. (Posner, 1980). If PSZ had an impaired ability to focus attention, This article is intended solely for the personal use of the individual userSteven and is not to be disseminated broadly. J. Luck and Clara McClenon, Center for Mind & Brain and Department of Psychology, University of California, Davis; Valerie M. then they should exhibit a smaller difference in performance Beck, Department of Psychology, University of Iowa and Center for Mind between valid and invalid trials, but this validity effect is generally & Brain and Department of Psychology, University of California, Davis; unimpaired in PSZ (Gold et al., 2006; Gold, Hahn, Strauss, & Andrew Hollingworth, Department of Psychology, University of Iowa; Waltz, 2009; Hahn, Hollingworth et al., 2012). Moreover, a widely Carly J. Leonard, Center for Mind & Brain and Department of Psychology, University of California, Davis; Britta Hahn, Benjamin M. Robinson, and James M. Gold, Maryland Psychiatric Research Center, University of 1 Maryland School of Medicine. We use the term intensity to describe the level of activation of a This study was made possible by Grant R01MH065034 from the Na- representation (which may be related to the firing rate of the neurons that code the representation). We have avoided the term strength, because tional Institute of Mental Health to JMG and SJL and by Grant greater strength might imply a greater resistance to distraction, whereas R01EY017356 from the National Eye Institute to AH. greater intensity (a higher activation level) does not necessarily mean that Correspondence concerning this article should be addressed to Steven J. the representation is more robust. However, greater intensity of one rep- Luck, UC-Davis Center for Mind and Brain, 267 Cousteau Place, Davis, resentation would presumably increase the ability of this representation to CA 95618. E-mail: [email protected] compete or interfere with other concurrent representations. 783 784 LUCK ET AL. replicated finding is that the performance benefit of valid cues example, subjects are sometimes tested on the uncued items, and relative to spatially nonpredictive cues is often greater in PSZ than intense focusing on the cued item may therefore be suboptimal. in HCS (Bustillo et al., 1997; Gold et al., 1992; Hahn, Holling- This is the sort of situation in which we would predict that PSZ worth et al., 2012; Liotti, Dazzi, & Umilta, 1993; Sapir, Henik, would exhibit more intense focusing than HCS. As another exam- Dobrusin, & Hochman, 2001; Spencer et al., 2011). This finding of ple, consider the attentional blink paradigm, in which subjects see enhanced cue validity suggests that PSZ hyperfocus on the cued a rapid stream of items and must identify two targets within the location on valid trials or fail to distribute attention effectively on stream. Focusing attention onto the first target leads to a failure to neutral trials. detect the second target (an attentional blink), and studies of In WM studies, PSZ reliably exhibit reduced storage capacity healthy young adults have found that greater focusing on the first (Lee & Park, 2005; Piskulic, Olver, Norman, & Maruff, 2007). target leads to a larger or longer-lasting attentional blink (MacLean There are many possible explanations for this impairment, but a & Arnell, 2011; Shapiro, Schmitz, Martens, Hommel, & Schnit- recent event-related potential (ERP) study provided evidence that zler, 2006). Similarly, PSZ exhibit an exaggerated attentional blink the deficit arises because PSZ tend to devote more processing (Cheung, Chen, Chen, Woo, & Yee, 2002; Mathis, Wynn, Breit- resources to a smaller number of items (Leonard, Kaiser et al., meyer, Nuechterlein, & Green, 2011; Wynn, Breitmeyer, Nuech- 2013). Participants in this study were instructed to encode the terlein, & Green, 2006), consistent with the idea that they are items on one side of the display and to ignore the other side. This hyperfocusing on the first target and therefore failing to detect the made it possible to record the contralateral delay activity (CDA), second target. It should be noted that most of the research on this an ERP component that reflects the WM resources devoted to the topic has been performed with chronic, medicated, clinically stable cued side (Vogel & Machizawa, 2004; Vogel, McCollough, & outpatients, and we do not yet know if the proposed hyperfocusing Machizawa, 2005). When the cued side contained only one item, pattern is also present in other subpopulations of PSZ. PSZ exhibited a larger CDA than did HCS, indicating that PSZ The hyperfocusing hypothesis leads to a counterintuitive pre- allocated more resources to the cued side than did HCS (hyperfo- diction: Although PSZ are less likely to hold a given object in WM cusing on the cued side). In contrast, PSZ exhibited reduced CDA because of encoding failures (Lee & Park, 2005), the WM repre- amplitude (and impaired behavioral performance) when asked to sentations of PSZ will be more intense than those of HCS when a store three or five items in WM. This would be expected if HCS WM representation is actually present. This prediction follows could easily divide their resources among multiple items, whereas directly from the finding that the ERP signature of WM mainte- PSZ focused narrowly on only a small subset of the to-be- nance—the CDA—is significantly larger in PSZ than in HCS remembered items. In addition, the larger CDA in PSZ for 1-item when a single item is being stored in WM (Leonard, Kaiser et al., arrays was found even for subgroups of PSZ and HCS who were 2013). Testing this prediction is complicated by the fact that many matched for overall WM capacity, showing that it was not an cognitive processes are impaired in PSZ, such as global lapses of artifact of differences in capacity. attention (Barch et al., 2012), and this may artifactually create the Evidence of hyperfocusing has also been observed in experi- appearance of weaker WM representations. Thus, PSZ might ex- ments that combined attentional manipulations with WM encod- hibit a lower likelihood of maintaining an object in WM and yet ing. In one series of experiments (Gold et al., 2006), participants still have more intense WM representations for the subset of trials were cued to a subset of the items in an array; memory for the cued on which the object is present in WM. To test the strength of the items was tested on most trials (valid trials), but memory for the WM representations, it is therefore necessary to have a means of uncued items was tested on a subset of trials (invalid trials). When measuring the strength selectively for the trials on which a repre- the arrays contained two cued items and two uncued items, PSZ sentation is present.