Mesolimbic lipid sensing and the regulation of feeding behaviour

In both developed and emerging countries, sedentary life style and over exposition to high energy dense foods has led to a thermodynamic imbalance and consequently obesity. Despite genetic predisposition, obesity often involves a behavioral component in which, similar to drugs of abuse, compulsive consumption of palatable food rich in lipids and sugar drives energy intake far beyond metabolic demands. Food intake is modulated by sensory inputs, such as tastes and odours, as well as by affective or emotional states. The mesolimbic pathway is well established as a main actor of the rewarding aspect of feeding. Particularly, the hedonic and motivational aspects of food are closely tied to the release of the neurotransmitter dopamine (DA) in striatal structure such as the Nucleus Accumbens (Nacc). In both rodent and humans several studies shows an attenuated activity of dopaminergic signal associated with obesity and there is evidence that consumption of palatable food per se leads to DA signalling alterations. Furthermore impaired cognition in obese mice is improved by selectively lowering triglycerides (TG) and intracerebroventricular administration of TG induces by itself acquisition impairment in several cognitive paradigms in normal body weight mice. Together, these observations raise the possibility that nutritional lipids, particularly TG, directly affect cognitive and reward processes by modulating the mesolimbic pathway and might contribute to the downward spiral of compulsive consumption of palatable and obesity. This review is an attempt to capture recent evolution in the field that might point toward a direct action of nutritional lipid in the mesolimbic pathway.

[1]  R. Eckel,et al.  Dietary triglycerides act on mesolimbic structures to regulate the rewarding and motivational aspects of feeding , 2014, Molecular Psychiatry.

[2]  S. Luquet,et al.  Physiological and pathophysiological implications of lipid sensing in the brain , 2014, Diabetes, obesity & metabolism.

[3]  I. Araújo,et al.  The neural signature of satiation is associated with ghrelin response and triglyceride metabolism , 2014, Physiology & Behavior.

[4]  S. Luquet,et al.  Central orchestration of peripheral nutrient partitioning and substrate utilization: implications for the metabolic syndrome. , 2014, Diabetes & metabolism.

[5]  C. Magnan,et al.  Lipid sensing in the brain and regulation of energy balance. , 2014, Diabetes & metabolism.

[6]  S. Fulton,et al.  Metabolic disturbances connecting obesity and depression , 2013, Front. Neurosci..

[7]  Marina Sergeeva,et al.  Peroxisome proliferator-activated receptor (PPAR)β/δ, a possible nexus of PPARα- and PPARγ-dependent molecular pathways in neurodegenerative diseases: Review and novel hypotheses , 2013, Neurochemistry International.

[8]  C. Magnan,et al.  Fatty Acid Transporter CD36 Mediates Hypothalamic Effect of Fatty Acids on Food Intake in Rats , 2013, PloS one.

[9]  C. Magnan,et al.  FAT/CD36: A Major Regulator of Neuronal Fatty Acid Sensing and Energy Homeostasis in Rats and Mice , 2013, Diabetes.

[10]  R. Eckel,et al.  Lipoprotein lipase in the brain and nervous system. , 2012, Annual review of nutrition.

[11]  S. Subramanian,et al.  Hypertriglyceridemia secondary to obesity and diabetes. , 2012, Biochimica et biophysica acta.

[12]  G. Hatch,et al.  Fatty acid transport into the brain: of fatty acid fables and lipid tails. , 2011, Prostaglandins, leukotrienes, and essential fatty acids.

[13]  C. Magnan,et al.  Brain lipid sensing and nervous control of energy balance. , 2011, Diabetes & metabolism.

[14]  L. Velloso,et al.  Altered hypothalamic function in diet-induced obesity , 2011, International Journal of Obesity.

[15]  O. Manzoni,et al.  Nutritional omega-3 deficiency abolishes endocannabinoid-mediated neuronal functions , 2011, Nature Neuroscience.

[16]  N. Volkow,et al.  Reward, dopamine and the control of food intake: implications for obesity , 2011, Trends in Cognitive Sciences.

[17]  R. Eckel,et al.  Deficiency of lipoprotein lipase in neurons modifies the regulation of energy balance and leads to obesity. , 2011, Cell metabolism.

[18]  S. Eaton,et al.  Lipoprotein Particles Cross the Blood–Brain Barrier in Drosophila , 2010, The Journal of Neuroscience.

[19]  Gary J. Schwartz,et al.  Hypothalamic nutrient sensing in the control of energy homeostasis , 2010, Behavioural Brain Research.

[20]  P. Kenny,et al.  Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats , 2010, Nature Neuroscience.

[21]  S. Leibowitz,et al.  Circulating triglycerides after a high-fat meal: Predictor of increased caloric intake, orexigenic peptide expression, and dietary obesity , 2009, Brain Research.

[22]  K. Befort,et al.  Reward processing by the opioid system in the brain. , 2009, Physiological reviews.

[23]  R. Eckel,et al.  Lipoprotein lipase: from gene to obesity. , 2009, American journal of physiology. Endocrinology and metabolism.

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

[25]  C. Magnan,et al.  Characteristics and mechanisms of hypothalamic neuronal fatty acid sensing. , 2009, American journal of physiology. Regulatory, integrative and comparative physiology.

[26]  F. Karpe,et al.  Fasted to fed trafficking of Fatty acids in human adipose tissue reveals a novel regulatory step for enhanced fat storage. , 2009, The Journal of clinical endocrinology and metabolism.

[27]  A. Vidal-Puig,et al.  AMPK: a metabolic gauge regulating whole-body energy homeostasis. , 2008, Trends in molecular medicine.

[28]  Y. Loh,et al.  Faculty Opinions recommendation of Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. , 2008 .

[29]  M. Karin,et al.  Hypothalamic IKKβ/NF-κB and ER Stress Link Overnutrition to Energy Imbalance and Obesity , 2008, Cell.

[30]  R. Bazinet,et al.  Regulation of brain polyunsaturated fatty acid uptake and turnover. , 2008, Prostaglandins, leukotrienes, and essential fatty acids.

[31]  L. Fenart,et al.  Physiological pathway for low-density lipoproteins across the blood-brain barrier: transcytosis through brain capillary endothelial cells in vitro. , 2008, Endothelium : journal of endothelial cell research.

[32]  D. Piomelli,et al.  The endocannabinoid system in brain reward processes , 2008, British journal of pharmacology.

[33]  R. Palmiter Dopamine Signaling in the Dorsal Striatum Is Essential for Motivated Behaviors , 2008, Annals of the New York Academy of Sciences.

[34]  N. E. Miller,et al.  Obesity and hypertriglyceridemia produce cognitive impairment. , 2008, Endocrinology.

[35]  C. Lelliott,et al.  Acutely reduced locomotor activity is a major contributor to Western diet-induced obesity in mice. , 2008, American journal of physiology. Endocrinology and metabolism.

[36]  R. Palmiter Is dopamine a physiologically relevant mediator of feeding behavior? , 2007, Trends in Neurosciences.

[37]  Giuseppe Esposito,et al.  Imaging signal transduction via arachidonic acid in the human brain during visual stimulation, by means of positron emission tomography , 2007, NeuroImage.

[38]  G. Simpson,et al.  Weight Gain During a Double-Blind Multidosage Clozapine Study , 2007, Journal of clinical psychopharmacology.

[39]  A. Kelley,et al.  Pharmacological characterization of high-fat feeding induced by opioid stimulation of the ventral striatum , 2006, Physiology & Behavior.

[40]  G. Ronnett,et al.  Fatty Acid Metabolism, the Central Nervous System, and Feeding , 2006, Obesity.

[41]  Karine Clément,et al.  Genetics of human obesity. , 2006, The Proceedings of the Nutrition Society.

[42]  R. Wise Role of brain dopamine in food reward and reinforcement , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[43]  O. Valverde,et al.  Involvement of the endocannabinoid system in drug addiction , 2006, Trends in Neurosciences.

[44]  A. Kelley,et al.  A proposed hypothalamic–thalamic–striatal axis for the integration of energy balance, arousal, and food reward , 2005, The Journal of comparative neurology.

[45]  M. J. Vazquez,et al.  Sensing the fat: Fatty acid metabolism in the hypothalamus and the melanocortin system , 2005, Peptides.

[46]  M. Ajmal,et al.  CD36 expression and brain function: does CD36 deficiency impact learning ability? , 2005, Prostaglandins & other lipid mediators.

[47]  G. Ronnett,et al.  Fatty acid metabolism as a target for obesity treatment , 2005, Physiology & Behavior.

[48]  L. Rossetti,et al.  Hypothalamic sensing of fatty acids , 2005, Nature Neuroscience.

[49]  D. Porte,et al.  Diabetes, Obesity, and the Brain , 2005, Science.

[50]  P. Vallet,et al.  Lipoprotein lipase and endothelial lipase expression in mouse brain: regional distribution and selective induction following kainic acid-induced lesion and focal cerebral ischemia , 2004, Neurobiology of Disease.

[51]  L. Epstein,et al.  Influence of methylphenidate on eating in obese men. , 2004, Obesity research.

[52]  S. L. la Fleur,et al.  Chronic stress and obesity: A new view of “comfort food” , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Alain Dagher,et al.  Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers , 2003, NeuroImage.

[54]  James O. Hill,et al.  Obesity and the Environment: Where Do We Go from Here? , 2003, Science.

[55]  Richard E Carson,et al.  Brain Incorporation of [11C]Arachidonic Acid in Young Healthy Humans Measured with Positron Emission Tomography , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[56]  C. Townsend,et al.  Expression of FAS within hypothalamic neurons: a model for decreased food intake after C75 treatment. , 2002, American journal of physiology. Endocrinology and metabolism.

[57]  S. Haber,et al.  Opioid modulation of taste hedonics within the ventral striatum , 2002, Physiology & Behavior.

[58]  Monica V. Kumar,et al.  Differential effects of a centrally acting fatty acid synthase inhibitor in lean and obese mice , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Zhaohui Feng,et al.  Central administration of oleic acid inhibits glucose production and food intake. , 2002, Diabetes.

[60]  S. Rapoport,et al.  Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. , 2001, Journal of lipid research.

[61]  R. Palmiter,et al.  Dopamine Production in the Caudate Putamen Restores Feeding in Dopamine-Deficient Mice , 2001, Neuron.

[62]  Stanley I. Rapoport,et al.  In vivo fatty acid incorporation into brain phosholipids in relation to plasma availability, signal transduction and membrane remodeling , 2001, Journal of Molecular Neuroscience.

[63]  J. Edmond Essential polyunsaturated fatty acids and the barrier to the brain , 2001, Journal of Molecular Neuroscience.

[64]  H. Nagura,et al.  Fatty acid uptake and incorporation in brain , 2001, Journal of Molecular Neuroscience.

[65]  F. Bellisle,et al.  Palatability and intake relationships in free-living humans characterization and independence of influence in North Americans , 2000, Physiology & Behavior.

[66]  F. Bellisle,et al.  Palatability and intake relationships in free-living humans measurement and characterization in the French , 2000, Physiology & Behavior.

[67]  R. Palmiter,et al.  Viral Gene Delivery Selectively Restores Feeding and Prevents Lethality of Dopamine-Deficient Mice , 1999, Neuron.

[68]  Peter Herscovitch,et al.  Brain incorporation of [1–11C]arachidonate in normocapnic and hypercapnic monkeys, measured with positron emission tomography , 1997, Brain Research.

[69]  M. Chang,et al.  Incorporation of [U-14C]palmitate into rat brain: effect of an inhibitor of beta-oxidation. , 1997, Journal of lipid research.

[70]  S. Rapoport,et al.  Incorporation of [1-carbon-11]palmitate in monkey brain using PET. , 1995, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[71]  G. P. Smith,et al.  Raclopride decreases sucrose intake of rat pups in independent ingestion tests , 1992, Pharmacology Biochemistry and Behavior.

[72]  C. Chang,et al.  Synthesis and regulation of lipoprotein lipase in the hippocampus. , 1990, Journal of lipid research.

[73]  R. Eckel,et al.  Lipoprotein lipase is produced, regulated, and functional in rat brain. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[74]  G. W. Reid,et al.  Relative palatability to sheep of straw, hay and dried grass , 1971, British Journal of Nutrition.

[75]  H. Moser,et al.  Brain uptake and utilization of fatty acids , 2007, Journal of Molecular Neuroscience.

[76]  J. M. de Castro Palatability and intake relationships in free-living humans: the influence of heredity. , 2001, Nutrition research.