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Increased Brain Response to Appetitive Tastes in the Insula and Amygdala in Obese Compared with Healthy Weight Children When Sated

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Increased Brain Response to Appetitive Tastes in the Insula and Amygdala in Obese Compared with Healthy Weight Children When Sated International Journal of Obesity (2015) 39, 620–628 © 2015 Macmillan Publishers Limited All rights reserved 0307-0565/15 www.nature.com/ijo PEDIATRIC ORIGINAL ARTICLE Increased brain response to appetitive tastes in the insula and amygdala in obese compared with healthy weight children when sated KN Boutelle1,2, CE Wierenga1,3, A Bischoff-Grethe1, AJ Melrose1, E Grenesko-Stevens1, MP Paulus1,3 and WH Kaye1 OBJECTIVE: There is evidence of altered neural taste response in female adolescents who are obese (OB), and in adolescents who are at risk for obesity. To further understand risk factors for the development of overeating and obesity, we investigated response to tastes of sucrose and water in 23 OB and healthy weight (HW) children. METHODS AND DESIGN: Thirteen HW and 10 OB 8–12-year-old children underwent functional magnetic resonance imaging while tasting sucrose and water. Additionally, children completed an eating in the absence of hunger paradigm and a sucrose-liking task. RESULTS: A region of interest analysis revealed an elevated BOLD response to taste (sucrose and water) within the bilateral insula and amygdala in OB children relative to HW children. Whole-brain analyses revealed a group by condition interaction within the paracingulate, medial frontal, middle frontal gyri and right amygdala: post hoc analyses suggested an increased response to sucrose for OB relative to HW children, whereas HW children responded more strongly to water relative to sucrose. In addition, OB children, relative to HW, tended to recruit the right putamen as well as medial and lateral frontal and temporal regions bilaterally. CONCLUSION: This study showed increased reactivity in the amygdala and insula in the OB compared with HW children, but no functional differentiation in the striatum, despite differences in the striatum previously seen in older samples. These findings support the concept of the association between increased neural processing of food reward in the development of obesity, and raise the possibility that emotional and interoceptive sensitivity could be an early vulnerability in obesity. International Journal of Obesity (2015) 39, 620–628; doi:10.1038/ijo.2014.206 INTRODUCTION increase in neural processing of food reward.12 Others have Approximately one-third of children in the United States are proposed that those at risk for obesity have an initial hyperreac- overweight or obese (OB),1 affecting 4–5 million children. Children tivity in the striatum and somatosensory and gustatory regions, who are OB are at an increased risk for negative health sequelae in which drives overeating. Over time, there is a decrease in striatal childhood and adulthood, including orthopedic and endo- response and increases in regions that encode incentive salience crine conditions, cardiovascular disease, cancer and all-cause of food cues, which leads to further overeating and weight 13,14 mortality.2–5 Unfortunately, obesity tracks well from childhood to gain. All of these models implicate neural regions associated adolescence and adulthood, with over 80% of OB youth remaining with dopamine functioning, including the striatum, mesolimbic OB in adulthood.6 pathway and mesocortical pathways.15,16 The primary gustatory Although several factors contribute to weight gain, eating pathway, which partially overlaps with the above circuits but above and beyond daily caloric requirements plays a primary extends to the insula, is responsible for the integration of sensory etiological role in obesity across the life span.7 Appetite regulation information and taste from the mouth. Additionally, the insula has as a whole is a complex process that involves the integration of been implicated in the anticipation of reward and outcomes.17,18 multiple physiological signals, including energy needs in the body, Together with the anterior cingulate cortex and orbitofrontal neural processes and cognitive processes. Neural mechanisms, in cortex, the insula codes the sensory-hedonic response to taste, is particular motivation and reward, are considered central compo- implicated in the anticipation of outcomes and innervates a broad – nents in regulating eating behavior.8 Recent studies of obesity region of the rostral ventral-central striatum.19 22 This network suggest that top-down neural processes, which encode the is thought to play a crucial role in linking sensory-hedonic rewarding, emotional and cognitive aspects of food ingestion, experiences to the motivational components of reward19 that may may lead to important understandings of why some individuals govern eating behavior. over-consume food, even in the presence of satiety and replete The functional development of these regions is not well energy stores.9,10 understood, and very little is known about the development of A number of models regarding the neural processes of obesity the reward pathways in childhood, let alone about the reward and overeating have been proposed. One model suggests that OB pathways related to taste and food consumption. Studying compared with normal weight people have decreased neural taste reward in children earlier in life will allow for a processing of food reward,11 whereas another suggests an greater understanding of the conflicting reports of the hypo- vs 1University of California San Diego, Department of Psychiatry, La Jolla, CA, USA; 2University of California San Diego, Department of Pediatrics, La Jolla, CA, USA and 3Veterans Affairs San Diego Healthcare System, Research Service, San Diego, CA, USA. Correspondence: Dr KN Boutelle, Department of Pediatrics and Psychiatry, University of California, San Diego, 8950 Villa La Jolla Dr Suite A203, La Jolla, CA 92037, USA. E-mail: [email protected] Received 2 April 2014; revised 17 October 2014; accepted 10 November 2014; accepted article preview online 11 December 2014; advance online publication, 13 January 2015 Brain response to appetitive tastes KN Boutelle et al 621 hyper-reward sensitivity seen in obesity. Understanding the METHODS development of the taste reward pathways in childhood is crucial Subjects for understanding the development of reward over the life span Ten OB children (5 boys, 5 girls) aged 8–12 (body mass index (BMI) and will assist in the development of interventions to address percentile 495th for age) were recruited from the community. Thirteen overeating. age-matched HW (BMIo85th%) children (8 boys, 5 girls) were recruited To date, there are relatively few studies evaluating the neural through local advertisements and pediatric clinics. Inclusion criteria responsivity to food in OB and healthy weight (HW) youth, and included willingness to participate in the study, meeting weight criteria fl these studies have used paradigms that include both pictures of for the two groups (OB or HW), right-handedness, uent in English (for 23,24 25,26 speaking, reading and writing) and liking of cheese pizza (necessary to food and food delivery to assess reward, motivation and complete the Eating in the Absence of Hunger (EAH) assessment). interoceptive circuitry. The studies that have evaluated the Exclusion criteria included any eating disorder (diagnosed by chEDE-C)31 delivery of reward have compared the taste of chocolate or other significant psychiatric disorder (MINI-kid),32 or other medical or milkshake and tasteless solution in OB and HW female adoles- neurologic concerns and conditions contraindicative to magnetic reso- cents. Results indicated that OB compared with HW teens showed nance imaging (MRI). Child height was measured using a portable Schorr increased activation in the gustatory cortex (anterior and mid height board (Schorr Inc, Olney, MD, USA) in duplicate. Height was insula, frontal operculum) and in the somatosensory regions recorded to the nearest 0.1 cm for both trials. Body weight in kilograms was measured in duplicate on a Tanita Digital Scale (model WB-110A; (parietal operculum and rolandic operculum) in anticipation of Tanita Corporation of America, Inc., Arlington Heights, IL, USA). Body consumption of a chocolate milkshake compared with actual weight was recorded to the nearest 0.1 kg. The average of the two values consumption. However, OB compared with HW females showed for height and weight was converted to BMI (BMI = [kg m − 2]). Because decreased activation in the caudate nucleus in response to children are growing, BMI was translated to BMI for age percentile score 33 consumption of chocolate milkshake compared with a tasteless using the CDC growth charts. solution.25 Another study by the same group compared normal The study was conducted according to the Institutional Review Board regulations of the University of California, San Diego. Participants gave weight female adolescents determined to be at high or low risk of ’ written informed assent, and their parents gave written informed consent. obesity (based on parent s obesity status) and found that Participants completed an EAH evaluation and a Monell forced-choice adolescents at high risk for obesity showed activation in the paired-comparison task for assessing sweet taste preference (that is, caudate, parietal operculum and frontal operculum in response to sucrose liking). Between group comparisons of assessment scores were chocolate milkshake compared with a tasteless solution,26 performed using Student’s t-tests and assumed unequal variance when suggesting that many of these neural changes may exist prior indicated (Table 1). to adolescence and prior to obesity onset. To date, there are no data on food reward delivery in younger
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