The Impact of Caloric and Non-Caloric Sweeteners on Food Intake and Brain Responses to Food: A Randomized Crossover Controlled Trial in Healthy Humans

Whether non-nutritive sweetener (NNS) consumption impacts food intake behavior in humans is still unclear. Discrepant sensory and metabolic signals are proposed to mislead brain regulatory centers, in turn promoting maladaptive food choices favoring weight gain. We aimed to assess whether ingestion of sucrose- and NNS-sweetened drinks would differently alter brain responses to food viewing and food intake. Eighteen normal-weight men were studied in a fasted condition and after consumption of a standardized meal accompanied by either a NNS-sweetened (NNS), or a sucrose-sweetened (SUC) drink, or water (WAT). Their brain responses to visual food cues were assessed by means of electroencephalography (EEG) before and 45 min after meal ingestion. Four hours after meal ingestion, spontaneous food intake was monitored during an ad libitum buffet. With WAT, meal intake led to increased neural activity in the dorsal prefrontal cortex and the insula, areas linked to cognitive control and interoception. With SUC, neural activity in the insula increased as well, but decreased in temporal regions linked to food categorization, and remained unchanged in dorsal prefrontal areas. The latter modulations were associated with a significantly lower total energy intake at buffet (mean kcal ± SEM; 791 ± 62) as compared to WAT (942 ± 71) and NNS (917 ± 70). In contrast to WAT and SUC, NNS consumption did not impact activity in the insula, but led to increased neural activity in ventrolateral prefrontal regions linked to the inhibition of reward. Total energy intake at the buffet was not significantly different between WAT and NNS. Our findings highlight the differential impact of caloric and non-caloric sweeteners on subsequent brain responses to visual food cues and energy intake. These variations may reflect an initial stage of adaptation to taste-calorie uncoupling, and could be indicative of longer-term consequences of repeated NNS consumption on food intake behavior.

[1]  M. Murray,et al.  The impact of replacing sugar- by artificially-sweetened beverages on brain and behavioral responses to food viewing – An exploratory study , 2018, Appetite.

[2]  E. Franz,et al.  The “sweet” effect: Comparative assessments of dietary sugars on cognitive performance , 2018, Physiology & Behavior.

[3]  Jair C. Soares,et al.  Inhibitory control in obesity and binge eating disorder: A systematic review and meta-analysis of neurocognitive and neuroimaging studies , 2016, Neuroscience & Biobehavioral Reviews.

[4]  S. Simpson,et al.  Sucralose Promotes Food Intake through NPY and a Neuronal Fasting Response. , 2016, Cell metabolism.

[5]  Rajita Sinha,et al.  Altered Brain Response to Drinking Glucose and Fructose in Obese Adolescents , 2016, Diabetes.

[6]  D. Small,et al.  Physiological mechanisms by which non-nutritive sweeteners may impact body weight and metabolism , 2015, Physiology & Behavior.

[7]  O. Bruyère,et al.  Erratum to: Review of the nutritional benefits and risks related to intense sweeteners , 2015, Archives of Public Health.

[8]  Yueqing Peng,et al.  Sweet and bitter taste in the brain of awake behaving animals , 2015, Nature.

[9]  Micah M. Murray,et al.  Brain dynamics of meal size selection in humans , 2015, NeuroImage.

[10]  R. Cela,et al.  Determination of artificial sweeteners in beverages with green mobile phases and high temperature liquid chromatography-tandem mass spectrometry. , 2015, Food chemistry.

[11]  Bruyère Olivier,et al.  Review of the nutritional benefits and risks related to intense sweeteners. , 2015, Archives of public health = Archives belges de sante publique.

[12]  Loïc Briand,et al.  Functional roles of the sweet taste receptor in oral and extraoral tissues , 2014, Current opinion in clinical nutrition and metabolic care.

[13]  E. Mayer,et al.  Influence of sucrose ingestion on brainstem and hypothalamic intrinsic oscillations in lean and obese women. , 2014, Gastroenterology.

[14]  Micah M. Murray,et al.  Verbal labels selectively bias brain responses to high-energy foods , 2014, NeuroImage.

[15]  Thorsten Kahnt,et al.  The role of neural impulse control mechanisms for dietary success in obesity , 2013, NeuroImage.

[16]  A. Harris,et al.  Temporally Dissociable Mechanisms of Self-Control: Early Attentional Filtering Versus Late Value Modulation , 2013, The Journal of Neuroscience.

[17]  P. Shankar,et al.  Non-nutritive sweeteners: review and update. , 2013, Nutrition.

[18]  S. Swithers.  Artificial sweeteners produce the counterintuitive effect of inducing metabolic derangements , 2013, Trends in Endocrinology & Metabolism.

[19]  E. Mayer,et al.  Differences in brain responses between lean and obese women to a sweetened drink , 2013, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[20]  D. Small.  Flavor is in the brain , 2012, Physiology & Behavior.

[21]  C. Murphy,et al.  Altered processing of sweet taste in the brain of diet soda drinkers , 2012, Physiology & Behavior.

[22]  H. Berthoud.  The neurobiology of food intake in an obesogenic environment , 2012, Proceedings of the Nutrition Society.

[23]  A. Dagher.  Functional brain imaging of appetite , 2012, Trends in Endocrinology & Metabolism.

[24]  D. Small,et al.  Amygdala response to sucrose consumption is inversely related to artificial sweetener use , 2012, Appetite.

[25]  Micah M. Murray,et al.  The role of energetic value in dynamic brain response adaptation during repeated food image viewing , 2012, Appetite.

[26]  H. Berthoud.  Metabolic and hedonic drives in the neural control of appetite: who is the boss? , 2011, Current Opinion in Neurobiology.

[27]  Ashley A. Martin,et al.  Intake of High-Intensity Sweeteners Alters the Ability of Sweet Taste to Signal Caloric Consequences: Implications for the Learned Control of Energy and Body Weight Regulation , 2011, Quarterly journal of experimental psychology.

[28]  Max A. Viergever,et al.  The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues , 2011, NeuroImage.

[29]  D. Mitchell.  The nexus between decision making and emotion regulation: A review of convergent neurocognitive substrates , 2011, Behavioural Brain Research.

[30]  A. Villringer,et al.  Peptide hormones regulating appetite—focus on neuroimaging studies in humans , 2011, Diabetes/metabolism research and reviews.

[31]  Max A. Viergever,et al.  Consumption of caloric and non-caloric versions of a soft drink differentially affects brain activation during tasting , 2011, NeuroImage.

[32]  A. Renwick,et al.  Sweet-taste receptors, low-energy sweeteners, glucose absorption and insulin release , 2010, British Journal of Nutrition.

[33]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[34]  F. Hu,et al.  Contemporary Reviews in Cardiovascular Medicine Sugar-Sweetened Beverages, Obesity, Type 2 Diabetes Mellitus, and Cardiovascular Disease Risk , 2010 .

[35]  Shinsuke Shimojo,et al.  Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex decreases valuations during food choices , 2009, The European journal of neuroscience.

[36]  K. Berridge.  ‘Liking’ and ‘wanting’ food rewards: Brain substrates and roles in eating disorders , 2009, Physiology & Behavior.

[37]  D. Jones,et al.  Carbohydrate sensing in the human mouth: effects on exercise performance and brain activity , 2009, The Journal of physiology.

[38]  Micah M. Murray,et al.  The brain tracks the energetic value in food images , 2009, NeuroImage.

[39]  K. Hunt,et al.  Fueling the Obesity Epidemic? Artificially Sweetened Beverage Use and Long‐term Weight Gain , 2008, Obesity.

[40]  M. Stumvoll,et al.  Brain Activity in Hunger and Satiety: An Exploratory Visually Stimulated fMRI Study , 2008, Obesity.

[41]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[42]  M. Murray,et al.  Generating Controlled Image Sets in Cognitive Neuroscience Research , 2008, Brain Topography.

[43]  Martin P. Paulus,et al.  Sucrose activates human taste pathways differently from artificial sweetener , 2008, NeuroImage.

[44]  D. Ffytche,et al.  PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans , 2007, Nature.

[45]  Ralph B. D'Agostino,et al.  Soft Drink Consumption and Risk of Developing Cardiometabolic Risk Factors and the Metabolic Syndrome in Middle-Aged Adults in the Community , 2007, Circulation.

[46]  Á. Pascual-Leone,et al.  The right brain hypothesis for obesity. , 2007, JAMA.

[47]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[48]  K. Brownell,et al.  Effects of soft drink consumption on nutrition and health: a systematic review and meta-analysis. , 2007, American journal of public health.

[49]  J. V. Verhagen.  The neurocognitive bases of human multimodal food perception: Consciousness , 2007, Brain Research Reviews.

[50]  M. Kringelbach.  The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[51]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[52]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[53]  Piotr Bogorodzki,et al.  Cortical and limbic activation during viewing of high- versus low-calorie foods , 2003, NeuroImage.

[54]  R. Mattes,et al.  Liquid versus solid carbohydrate: effects on food intake and body weight , 2000, International Journal of Obesity.

[55]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[56]  E. Ravussin,et al.  Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[57]  L. Garfinkel,et al.  Patterns of artificial sweetener use and weight change in an American Cancer Society prospective study , 1988, Appetite.

[58]  F. Perrin,et al.  Mapping of scalp potentials by surface spline interpolation. , 1987, Electroencephalography and clinical neurophysiology.

[59]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[60]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.