n-Back task performance and corresponding brain-activation patterns in women with restrictive and bulimic eating-disorder variants: Preliminary findings

Highlights

• Working memory was shown to be influenced by eating disorder subtype.

• Working memory performance was poorer in women with binge-eating/purging behaviors.

• Group-based activation differences were noted in regions subserving executive function.

Abstract

Eating disorder (ED) variants characterized by “binge-eating/purging” symptoms differ from “restricting-only” variants along diverse clinical dimensions, but few studies have compared people with these different eating-disorder phenotypes on measures of neurocognitive function and brain activation. We tested the performances of 19 women with “restricting-only” eating syndromes and 27 with “binge-eating/purging” variants on a modified n-back task, and used functional magnetic resonance imaging (fMRI) to examine task-induced brain activations in frontal regions of interest. When compared with “binge-eating/purging” participants, “restricting-only” participants showed superior performance. Furthermore, in an intermediate-demand condition, “binge-eating/purging” participants showed significantly less event-related activation than did “restricting-only” participants in a right posterior prefrontal region spanning Brodmann areas 6–8—a region that has been linked to planning of motor responses, working memory for sequential information, and management of uncertainty. Our findings suggest that working memory is poorer in eating-disordered individuals with binge-eating/purging behaviors than in those who solely restrict food intake, and that observed performance differences coincide with interpretable group-based activation differences in a frontal region thought to subserve planning and decision making.

Introduction

Most diagnostic criteria for the eating disorders (EDs) differentiate anorexia nervosa (AN) from bulimia nervosa (BN) (e.g., American Psychiatric Association, 2013)—AN being characterized by willful restriction of food intake and weight loss, BN by recurrent eating binges and compensations (through self-induced vomiting, laxative misuse, or other means). As binge-eating and purging occur in many people with AN, the syndrome is further subdivided into “AN-restricting (AN-R)” and “AN-binge-eating/purging” (AN-BP) types, depending upon the presence or absence of binge-eating and purging behaviors. Individuals who binge and purge (whether they have AN-BP or BN) are noted to be more prone to behavioral disinhibition and affective instability than are those who solely restrict food intake (Rosval et al., 2006, Steiger et al., 2013, Wu et al., 2013), and various findings validate the concept that “restricting-only” and “binge-eating/purging” individuals, regardless of weight status, fall into separate classes (Keel et al., 2004, Williamson et al., 2005, Wade et al., 2006, Wildes and Marcus, 2013). The present study sought to evaluate the extent to which the “restricter-only” versus “binger–purger” distinction coincided with distinct neurocognitive tendencies.

Executive functions are higher order cognitive processes that regulate such mental operations as selective attention, working memory, and inhibitory control (Elliott, 2003). Executive functions are thought to implicate “frontostriatal” neurocircuits encompassing the dorsolateral prefrontal cortex (DLPFC), the anterior cingulate cortex, and connected brain structures—including the premotor and motor cortices, dorsal cingulate cortex, frontal poles, and medial posterior parietal cortex (Phillips et al., 2003). Some functional neuroimaging studies in ED populations point to the presence of frontostriatal abnormalities and associated executive-control problems (Pietrini et al., 2011, Friederich et al., 2013). For instance, Marsh and colleagues reported that adults with BN responded more impulsively and made more errors than did healthy adults on a task necessitating the inhibition of responses that were “primed” by incongruent stimulus information. Furthermore, when responding correctly to incongruent trials, people with BN failed to activate frontostriatal circuits to the extent seen in healthy controls (Marsh et al., 2009). Severity of bulimic symptoms was inversely correlated with the extent of frontal activations. A follow-up study in adolescents with BN roughly replicated the imaging findings, but not group-based performance differences, or the association between activations and eating symptoms (Marsh et al., 2011). Also implicating frontostriatal circuitry, but showing different activation patterns, a second study in adolescents found those with AN-BP or BN, when performing a go/no-go task tapping inhibitory control, to show significantly greater activations in the hypothalamus and right DLPFC than did healthy adolescents or adolescents with AN-R, and greater activations than did normal controls in the bilateral precentral gyri, anterior cingulate cortex, and middle and superior temporal gyri (Lock et al., 2011). Eating-symptom severity was not correlated with extent of activations.

n-Back tasks tap people׳s ability to maintain attentional control while manipulating task-relevant information in working memory (Owen et al., 2005, Kobel et al., 2009). Generally, n-back tests have participants respond to a target stimulus in accordance with a changing rule: “zero-back” conditions ask for a response to a target stimulus in the current trial, “1-back” to the stimulus׳ occurrence in the previous trial (i.e., one trial back), “2-back” to its occurrence two trials back, and so on. The n-back is presumed to primarily measure functionality of the prefrontal cortex (PFC) and connected structures—including the lateral premotor cortex, dorsal cingulate and medial premotor cortex, dorsolateral and ventrolateral PFC, frontal poles, and medial and lateral posterior parietal cortex (Owen et al., 2005, Rottschy et al., 2012). Some studies link working memory deficits with self-reported impulsiveness (Cheung et al., 2004, Stanford et al., 2009). Consistent with this notion, n-back performance is reported to be poor in people with borderline personality disorder (BPD: Hagenhoff et al., 2013), suicidality (Keilp et al., 2013), and attention-deficit/hyperactivity disorder (ADHD: McCarthy et al., 2014). When performing n-back tasks, ADHD patients reportedly activate bilateral middle frontal, cerebellar, occipital and parietal areas less than do controls (Valera et al., 2005, Bayerl et al., 2010). Likewise, on various tasks that recruit executive functions, BPD patients display hypoactivation of frontal areas—including the DLPFC (Krause-Utz et al., 2014). Additional findings suggest that acute stress hinders n-back performance, and dampens task-induced PFC (Porcelli and Delgado, 2009, Gärtner et al., 2014) and DLPFC (Qin et al., 2012) activations. Related to this point, emotional distraction has been observed to decrease working-memory task-induced DLPFC activation in BPD patients, but not in healthy individuals (Krause-Utz et al., 2012).

In ED populations, controlled studies have shown people with AN to display intact (Castro-Fornieles et al., 2010, Nikendei et al., 2011, Lao-Kaim et al., 2014) or even supra-normal n-back performance (Dickson et al., 2008, Brooks et al., 2012). Two studies have examined brain activations during n-back performance in participants with AN (although neither compared AN-R with AN-BP types): the first found adolescents with active AN to show greater task-induced activation in temporal and parietal areas than did controls (Castro-Fornieles et al., 2010). The second noted no activation differences between adults with or without AN (Lao-Kaim et al., 2014). No study, to date, has studied n-back performance in BN.

We compared n-back performance and corresponding brain activations between groups of “restricter-only” and “binger–purger” adults, using an n-back variant designed to tap performance across a range of working memory loads and stress conditions. The n-back in question, developed and used by a member of our group (J.P.), amalgamated standard n-back features tapping working memory (e.g., Owen et al., 2005) with stress-inducing features (see Dedovic et al. (2005)). The task was designed to push participants to their working memory limits, while incrementally adding task-induced stress. We reasoned that the challenge of maintaining executive controls under conditions of high cognitive load and stress might simulate real-life conditions conducive to dysregulation in susceptible individuals. Based on observations indicating good n-back performance in people with AN (Dickson et al., 2008, Brooks et al., 2012), and associating impulsivity with weaker working memory performance (Cheung et al., 2004, Stanford et al., 2009), we expected ED-R participants to show superior n-back performance to that of ED-BP participants. Of additional interest was to determine whether any observed performance differences coincided with PFC activation differences.

Given limited pilot funding available, we included no healthy comparison group, opting instead to optimize power to detect hypothetical differences between “restricter-only” and “binge-eating/purging” groups. We acknowledge that the lack of a healthy comparison group means that our study cannot localize findings relative to normative task performances and brain activations. Nonetheless, we felt that any observed “restricter”/“binger” differences as to neurocognitive function, especially if they corresponded to differences in brain activations, might help inform modeling of ED-subtype variations.