Altered Insula Response to Taste Stimuli in Individuals Recovered from Restricting-Type Anorexia Nervosa

Department of Psychiatry, School of Medicine, Western Psychiatric Institute and Clinic, University of Pittsburgh, Pittsburgh, PA 15213, USA.
Neuropsychopharmacology (Impact Factor: 7.05). 03/2008; 33(3):513-23. DOI: 10.1038/sj.npp.1301443
Source: PubMed


Anorexia nervosa (AN) is an illness characterized by aversion to ingestion of normally palatable foods. We examined whether there is a primary disturbance of taste processing and experience of pleasure using a sucrose/water task in conjunction with functional magnetic resonance imaging (fMRI). To avoid confounding effects of illness, 16 women recovered from restricting-type AN were compared to 16 control women (CW). We used a region of interest-based fMRI approach to test the idea that individuals with AN have differential neural activation in primary and secondary taste cortical regions after sucrose and water administration. Compared to CW, individuals recovered from AN showed a significantly lower neural activation of the insula, including the primary cortical taste region, and ventral and dorsal striatum to both sucrose and water. In addition, insular neural activity correlated with pleasantness ratings for sucrose in CW, but not in AN subjects. Altered taste processing may occur in AN, based on differences in activity in insular-striatal circuits. These data provide the first evidence that individuals with AN process taste stimuli differently than controls, based on differences in neural activation patterns.

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    • "This is a major research confound in that it becomes difficult to determine whether changes are a cause or consequence of starvation. Importantly, however, women recovered from AN often show incomplete normalisation of illness-related behaviours as well as altered neural reward processing of food cues [9,394041, suggesting that these alterations may reflect premorbid traits that contribute to illness vulnerability. Thus, to avoid confounding effects of malnutrition and to investigate state-vs trait-aspects of illness, we recruited AN REC and HC. "
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    ABSTRACT: This study investigated whether dopaminergic systems are involved in the motivation to engage in behaviours associated with anorexia nervosa (AN), specifically, the drive to exercise. Women recovered from AN (AN REC, n = 17) and healthy controls (HC, n = 15) were recruited. The acute phenylalanine/tyrosine depletion (APTD) method was used to transiently decrease dopamine synthesis and transmission. The effect of dopamine precursor depletion on drive to exercise was measured using a progressive ratio (PR) exercise breakpoint task. Both groups worked for the opportunity to exercise, and, at baseline, PR breakpoint scores were higher in AN REC than HC. Compared to values on the experimental control session, APTD did not decrease PR breakpoint scores in AN REC, but significantly decreased scores in HC. These data show that women recovered from AN are more motivated to exercise than HC, although in both groups, activity is more reinforcing than inactivity. Importantly, decreasing dopamine does not reduce the motivation to exercise in people recovered from AN, but in contrast, does so in HC. It is proposed that in AN, drive to exercise develops into a behaviour that is largely independent of dopamine mediated reward processes and becomes dependent on cortico-striatal neurocircuitry that regulates automated, habit- or compulsive-like behaviours. These data strengthen the case for the involvement of reward, learning, habit, and dopaminergic systems in the aetiology of AN.
    Full-text · Article · Jan 2016 · PLoS ONE
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    • "Studies on food cue-reactivity reported either insula hypo-[Gizewski et al., 2010; Holsen et al., 2012] or hyperactivity (Gizewski et al., 2010; Oberndorfer et al., 2013a) in patients with AN compared to HC. Two studies reported decreased insula responses to the oral application of sucrose as well as water in AN [Oberndorfer et al., 2013b; Wagner et al., 2008]. However, using a multimodal paradigm insula hyperactivation in AN was reported in response to aversive gustatory taste [Cowdrey et al., 2011]. "
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    ABSTRACT: The neural underpinnings of anorexia nervosa (AN) are poorly understood. Results from existing functional brain imaging studies using disorder-relevant food- or body-stimuli have been heterogeneous and may be biased due to varying compliance or strategies of the participants. In this study, resting state functional connectivity imaging was used. To explore the distributed nature and complexity of brain function we characterized network patterns in patients with acute AN. Thirty-five unmedicated female acute AN patients and 35 closely matched healthy female participants underwent resting state functional magnetic resonance imaging. We used a network-based statistic (NBS) approach [Zalesky et al., 2010a] to identify differences between groups by isolating a network of interconnected nodes with a deviant connectivity pattern. Group comparison revealed a subnetwork of connections with decreased connectivity including the amygdala, thalamus, fusiform gyrus, putamen and the posterior insula as the central hub in the patient group. Results were not driven by changes in intranodal or global connectivity. No network could be identified where AN patients had increased coupling. Given the known involvement of the identified thalamo-insular subnetwork in interoception, decreased connectivity in AN patients in these nodes might reflect changes in the propagation of sensations that alert the organism to urgent homeostatic imbalances and pain-processes that are known to be severely disturbed in AN and might explain the striking discrepancy between patient's actual and perceived internal body state. Hum Brain Mapp, 2015. © 2014 Wiley Periodicals, Inc.
    Full-text · Article · Jan 2015 · Human Brain Mapping
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    • "For example, Oberndorfer and colleagues found that compared to healthy controls, individuals recovered from AN showed increased activation of the anterior insula, an area of the brain involved in appetite and interoceptive regulation, during anticipation of food versus non-food stimuli (Oberndorfer, Simmons, et al., 2013). In line with our findings as well as studies from other groups (Wagner et al., 2008) subjective ratings of the food cues were not significantly correlated with activity in the insula in the recovered AN group, unlike in healthy controls, which suggests that in AN there may be a disconnect between subjective and objective interoceptive states which is exacerbated by food probes even after recovery from AN. "
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    ABSTRACT: Dysfunctional reward from the pursuit of thinness presents a major challenge to recovery from Anorexia Nervosa (AN). We explore the neuroscientific basis of aberrant reward in AN, with the aim of generating novel hypotheses for translational investigation, and elucidate disease mechanisms to inform the development of targeted interventions. Relevant neuroimaging and behavioural studies are reviewed. These suggest that altered eating in AN may be a consequence of aberrant reward processing combined with exaggerated cognitive control. We consider evidence that such aberrant reward processing is reflected in the compulsive behaviours characterising AN, with substantial overlap in the neural circuits implicated in reward processing and compulsivity. Drawing on contemporary neuroscientific theories of substance dependence, processes underpinning the shift from the initially rewarding pursuit of thinness to extreme and compulsive weight control behaviours are discussed. It is suggested that in AN, weight loss behaviour begins as overtly rewarding, goal-directed and positively reinforced, but over time becomes habitual and increasingly negatively reinforced. Excessive habit formation is suggested as one underlying mechanism perpetuating compulsive behaviour. Ongoing research into the behavioural and neural basis of aberrant reward in AN is required to further elucidate mechanisms. We discuss clinical and transdiagnostic implications, and propose that future treatment innovation may benefit from the development of novel interventions targeting aberrant reward processing in AN.
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