Resting state hypothalamic response to glucose predicts glucose-induced attenuation in the ventral striatal response to food cues

Feeding behavior is regulated by a complex interaction of central nervous system responses to metabolic signals that reflect nutrient availability and to food cues that trigger appetitive responses. Prior work has shown that the hypothalamus is a key brain area that senses and responds to changes in metabolic signals, and exposure to food cues induces the activation of brain areas involved in reward processing. However, it is not known how the hypothalamic responses to changes in metabolic state are related to reward responses to food cues. This study aimed to understand whether changes in hypothalamic activity in response to glucose-induced metabolic signals are linked to food-cue reactivity within brain areas involved in reward processing. We combined two neuroimaging modalities (Arterial Spin Labeling and Blood Oxygen Level Dependent) to measure glucose-induced changes in hypothalamic cerebral blood flow (CBF) and food-cue task induced changes in brain activity within reward-related regions. Twenty-five participants underwent a MRI session following glucose ingestion and a subset of twenty individuals underwent an additional water session on a separate day as a control condition (drink order randomized). Hunger was assessed before and after drink consumption. We observed that individuals who had a greater reduction in hypothalamic CBF exhibited a greater reduction in left ventral striatum food cue reactivity (Spearman's rho = 0.46, P = 0.048) following glucose vs. water ingestion. These results are the first to use multimodal imaging to demonstrate a link between hypothalamic metabolic signaling and ventral striatal food cue reactivity.

[1]  John A Detre,et al.  Perfusion fMRI for functional neuroimaging. , 2005, International review of neurobiology.

[2]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[3]  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.

[4]  J. Fulford,et al.  Functional MRI of the hypothalamic response to an oral glucose load , 2012, Diabetologia.

[5]  Hubert Preissl,et al.  Resting‐state functional connectivity of the human hypothalamus , 2014, Human brain mapping.

[6]  Hubert Preissl,et al.  Differential effect of glucose ingestion on the neural processing of food stimuli in lean and overweight adults , 2014, Human brain mapping.

[7]  R. Buxton,et al.  Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II) , 1998 .

[8]  P. Bandettini,et al.  QUIPSS II with thin‐slice TI1 periodic saturation: A method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling , 1999, Magnetic resonance in medicine.

[9]  E M Reiman,et al.  Differential brain responses to satiation in obese and lean men. , 2000, Diabetes.

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

[11]  E. Bullmore,et al.  Leptin Regulates Striatal Regions and Human Eating Behavior , 2007, Science.

[12]  Eric Stice,et al.  Food reward system: current perspectives and future research needs , 2015, Nutrition reviews.

[13]  R. Buxton,et al.  Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling , 1997, NMR in biomedicine.

[14]  Paul A. M. Smeets,et al.  Functional MRI of human hypothalamic responses following glucose ingestion , 2005, NeuroImage.

[15]  J. Monterosso,et al.  Abdominal fat is associated with a greater brain reward response to high-calorie food cues in Hispanic women , 2013, Obesity.

[16]  Peter T. Fox,et al.  The temporal response of the brain after eating revealed by functional MRI , 2000, Nature.

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

[18]  Sam R. Miller,et al.  Distinct Modulatory Effects of Satiety and Sibutramine on Brain Responses to Food Images in Humans: A Double Dissociation across Hypothalamus, Amygdala, and Ventral Striatum , 2010, The Journal of Neuroscience.

[19]  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.

[20]  Emer Hughes,et al.  Fasting biases brain reward systems towards high‐calorie foods , 2009, The European journal of neuroscience.

[21]  P T Fox,et al.  Altered hypothalamic function in response to glucose ingestion in obese humans. , 1999, Diabetes.

[22]  A. Dagher,et al.  Food and drug cues activate similar brain regions: A meta-analysis of functional MRI studies , 2012, Physiology & Behavior.

[23]  E M Reiman,et al.  Effect of satiation on brain activity in obese and lean women. , 2001, Obesity research.

[24]  Hubert Preissl,et al.  Processing of food pictures: Influence of hunger, gender and calorie content , 2010, Brain Research.

[25]  William M. Kelley,et al.  Dietary Restraint Violations Influence Reward Responses in Nucleus Accumbens and Amygdala , 2011, Journal of Cognitive Neuroscience.

[26]  Kyle S. Burger,et al.  Caloric deprivation increases responsivity of attention and reward brain regions to intake, anticipated intake, and images of palatable foods , 2013, NeuroImage.

[27]  Uta Wolfensteller,et al.  (Still) longing for food: Insulin reactivity modulates response to food pictures , 2013, Human brain mapping.

[28]  J. Monterosso,et al.  Differential effects of fructose versus glucose on brain and appetitive responses to food cues and decisions for food rewards , 2015, Proceedings of the National Academy of Sciences.

[29]  Joana Ramalho,et al.  Arterial spin labeling in neuroimaging. , 2010, World journal of radiology.

[30]  A. Roebroeck,et al.  Behavioural Brain Research , 2015 .

[31]  R. Goebel,et al.  Increased sensitivity to food cues in the fasted state and decreased inhibitory control in the satiated state in the overweight. , 2013, The American journal of clinical nutrition.

[32]  Hengyi Rao,et al.  Arterial spin-labeled perfusion MRI in basic and clinical neuroscience , 2009, Current opinion in neurology.

[33]  M. V. van Osch,et al.  Functional magnetic resonance imaging of human hypothalamic responses to sweet taste and calories. , 2005, The American journal of clinical nutrition.

[34]  Alexander W. Johnson Eating beyond metabolic need: how environmental cues influence feeding behavior , 2013, Trends in Neurosciences.

[35]  R Todd Constable,et al.  Circulating glucose levels modulate neural control of desire for high-calorie foods in humans. , 2011, The Journal of clinical investigation.

[36]  Jason R. Tregellas,et al.  The Effects of Overfeeding on the Neuronal Response to Visual Food Cues in Thin and Reduced-Obese Individuals , 2009, PloS one.

[37]  Rachel K. Johnson,et al.  Comparison of multiple-pass 24-hour recall estimates of energy intake with total energy expenditure determined by the doubly labeled water method in young children. , 1996, Journal of the American Dietetic Association.

[38]  A. Nobre,et al.  Hunger selectively modulates corticolimbic activation to food stimuli in humans. , 2001, Behavioral neuroscience.

[39]  E. Ravussin,et al.  Neuroimaging and Obesity , 2002, Annals of the New York Academy of Sciences.

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

[41]  G. Aguirre,et al.  Experimental Design and the Relative Sensitivity of BOLD and Perfusion fMRI , 2002, NeuroImage.

[42]  C. Saper,et al.  The Need to Feed Homeostatic and Hedonic Control of Eating , 2002, Neuron.

[43]  Peter C M van Zijl,et al.  Theoretical and experimental investigation of the VASO contrast mechanism , 2006, Magnetic resonance in medicine.

[44]  R Todd Constable,et al.  Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. , 2013, JAMA.

[45]  Hubert Preissl,et al.  Insulin modulates food-related activity in the central nervous system. , 2010, The Journal of clinical endocrinology and metabolism.

[46]  M. Brammer,et al.  Cerebral processing of food-related stimuli: Effects of fasting and gender , 2006, Behavioural Brain Research.

[47]  Jeroen van der Grond,et al.  Glucose Ingestion Fails to Inhibit Hypothalamic Neuronal Activity in Patients With Type 2 Diabetes , 2007, Diabetes.

[48]  J. O'Doherty,et al.  Reward representations and reward-related learning in the human brain: insights from neuroimaging , 2004, Current Opinion in Neurobiology.

[49]  W. Teeuwisse,et al.  Hypothalamic BOLD response to glucose intake and hypothalamic volume are similar in anorexia nervosa and healthy control subjects , 2015, Front. Neurosci..

[50]  D Feskanich,et al.  Computerized collection and analysis of dietary intake information. , 1989, Computer methods and programs in biomedicine.

[51]  M. W. Schwartz,et al.  Central nervous system control of food intake and body weight , 2006, Nature.