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Is Obesity Caused by Food Addiction? Alain Dagher MD Montreal Neurological Institute McGill University Nothing in Biology Makes Sense Except in the Light of Evolution. - Theodosius Dobzhansky (1900-1975) Nothing in the Brain Makes Sense Except in the Light of Eating. Is hunger an addiction? • Homeostasis • Thirst determined by internal state • Homeostasis does not fully explain hunger • Calories can be stored • Water can’t be stored • Obtained through effort • Water doesn’t induce craving • Food can induce craving even • Easily available when satiated * • Hunger is learned * * Features of addiction Is hunger an addiction? • DO Hebb (1949) – “Salted peanuts” paradox. – Hunger and learning: Anxiety Reward • Initial effect of hunger is disruptive. • Infant learns that eating relieves unpleasant effects (e.g. stomach contractions). • Eventually hunger becomes an organized behaviour Empty Full • RA Wise (1978) – Dopamine blockade reduces the reinforcing and rewarding effects of food. – Addictive drugs act on brain circuitry that originally developed to serve feeding behaviour. stomach Feeding When is it an addiction? (DSM-IV) • A maladaptive pattern of substance use, leading to clinically significant impairment or distress, as manifested by three (or more) of the following, occurring at any time in the same 12-month period: – Tolerance – Withdrawal – Loss of control • Taken in larger amounts than intended • Persistent desire or unsuccessful efforts to cut down – Preoccupation – Important social, occupational, or recreational activities are given up or reduced – Continued use despite knowledge of adverse consequences Neurocognitive measures linked to obesity/appetite 66 64 51 50 – WCST 49 1 study 2 - 4 studies 5 - 7 studies 8 - 14 studies Mostly s 48 47 3 4 Motor Attention ma z 52 Time judge m Composite Inhibition 53 – ent 1 2 65 63 Fluency e Working memory Executive Visuospatial Language Semantic Shifting Memory Food motivation Complex 14 15 16 17 18 19 20 Episodic Decisionmaking Executive Implicit Attention control measures bias 21-79% s 34* 35 * 37* IAT 1 study ns 36* – 1 study s 30* 31* 32* 33* Mostly ns Vainik et al. Neurosci Biobehav Rev 2012 Stop Signal Reaction Time Task Nederkoorn et al. Health Psychology, 29(4), 389-393. 2010 Jansen et al. Behaviour Research and Therapy 2009 Personality (NEO-PI), Brain, Body weight Extraversion (sensitivity to reward) correlates with BMI Conscientiousness (planning, sticking to goals) predicts low BMI Brain Structure correlates of personality: (Self control) (Reward value) DeYoung et al. Psycho Sci 2010 fMRI studies of food reward I shouldn’t, but I’m going to have the garbage Brain response to “food cues” • Event-related fMRI • Images displayed 5s, 15s apart. hunger • Time since last meal • Energy balance (e.g. leptin, glucose) • Gut peptides (e.g. insulin, ghrelin) • Stress (acute, chronic) • Cognitive factors (e.g. selfcontrol) • Personality / Eating style time fMRI activation (“incentive salience”) 1 4 ++ + 2 3 Stimuli 5 ++ + 1. 2. 3. 4. 5. OFC Amygdala Visual areas Insula Lateral PFC Why study cues? • Cues cause relapse • Cues increase consumption • Neural response to cues predicts consumption and relapse • Cues are in the environment – Obesogenic environment – Role of public smoking regulations • Cues are Pavlovian conditioned stimuli • All foods are conditioned stimuli … A: Dopamine and conditioning 1 2 Reward (drug, food) Reward (drug, food) Conditioned stimulus 3 4 Conditioned stimulus Conditioned stimulus sensitization DOPAMINE Incentive Salience DOPAMINE Incentive Salience DOPAMINE Incentive Salience DOPAMINE Incentive Salience Approach (wanting, craving) Approach (wanting, craving) Approach (wanting, craving) Approach (wanting, craving) B: Conditioning to food Food Flavor Flavor Flavor Sight, smell Fuel sensing DOPAMINE DOPAMINE DOPAMINE Approach (wanting, craving) Approach (wanting, craving) Approach (wanting, craving) A Dagher, Trends Endo Metab, In Press The Appetitive Network • Cognitive control • Execution • Sensory specific satiety • Link cues to rewards • Assign value to stimuli & actions • Memory PFC / ACC • Ingestive cortex • Incentive learning • Role in drug craving Insula Amygdala OFC Striatum • Reward learning • Punishment learning • Transform motivation into action Smoking and food cues activate the appetitive network Food Amygdala OFC Insula Striatum Smoking Smoking (craving) Effect of ghrelin on cue response Ghrelin or Saline Malik et al., Cell Metab 2008 Gut - brain interactions Leptin ↓ Ghrelin ↑" Cota et al. Neuron 2006 Abizaid et al. JCI 2006 Ghrelin responsive areas Amygdala (-18 -10 -16) Fusiform Gyrus (-50 -66 -10) Insula (-34 20 8) Pulvinar (-18 -34 0) OFC (-28 30 -10) Malik et al. Cell Metab 2008 Ghrelin enhances memory saline p < 0.05 ghrelin n.s. Food cues and fMRI • Appetitive network cue response is greater in the hungry state. • Appetitive network response is modulated by ghrelin, PYY, leptin, insulin, glycemia. • Greater responsiveness in obese adults (N=5) and obese or at-risk children (N=3). • Reduced activation to food (milkshake) in obese – reward deficiency? A Dagher, Trends Endo Metab, In Press Consumer spending / GDP Marketing can overcome homeostasis • Hydration for health, an organization that promotes drinking water, has a mission to include drinking enough water as an integral part of public health nutritional guidelines and routine patient counseling so that patients can make informed choices. Appetite HOMEOSTATIC Blood glucose Leptin HEDONIC Sensory cues Food thoughts Vagus n. Gut peptides Hypothalamus Cerebral cortex Feeding Pleasure Allostasis • Homeostasis refers to error signal driven behavior • Allostasis proposed by Sterling and Eyer • Balance through behavioral adaptation • “Darwin's big idea: the goal of all species is not constancy of internal parameters but, rather, survival and reproduction.” – Peter Sterling (Physiology & Behavior, 2011) • Why pleasure? – To make predictions, create a model of the world for deciding Allostasis = anticipation of future needs Ghrelin, leptin, PYY, insulin, glucose Food cost Needs (energy balance) Opportunities ? Value Action Sterling and Eyer Neuroeconomics of obesity • In the developed world, obesity correlates somewhat with socio-economic status • Unhealthy energy-dense foods are cheaper than healthy foods, and energy density predicts palatability • Food consumed during a meal is determined at the planning stages. • Correlation between energy content of supermarket food purchases and daily caloric intake. • 40% of the recent increase in weight in America can be attributed to reduced food prices secondary to agricultural innovation and policy. Drewnowski and Eichelsdoerfer 2010 Price Elasticity Duffey et al. Arch Intern Med 2010 “Black Friday”, USA ca. 2005-2012 A new thrifty hypothesis • Thrifty gene selected in agricultural societies. • Cues signal abundance (low cost). • Low cost should trigger increased consumption. • Opportunity cost. • Consumption matched to cost. Prentice et al. Int J Obes 2008 Neuroeconomics of obesity How much would you pay for this item? $0 $1 $2 $3 $4 $5 Bid as a function of price and caloric density Bid vs caloric density ghrelin saline Price vs caloric density Ghrelin Increased Bidding for Food * { 2.5 Participant Bids * P < 0.05 * { 2 1.5 $ Saline Ghrelin 1 0.5 0 Food Trinket Overall vmPFC computes value Plassmann et al. J Neurosci 2007 2 Way Repeated Measures ANOVA Factors • Condition – Ghrelin/Saline • Run – 1, 2, 3, 4, 5, 6 F-map (Main effect of condition for food*bid) Ghrelin • Increases response to food cues in brain areas involved in motivation, hedonic evaluation, memory. • Increases willingness to pay for food. • Effect seen in the OFC/vmPFC area that computes value. Hunger and drugs • The development of feeding behaviour has similarities to drug addiction. – It is a learned behaviour – Not homeostatic • Food and drug cues activate brain areas involved in motivation, reward and attention. • Pharmacological treatments of obesity have a risk of causing psychiatric/mood side-effects. • Can lessons from tobacco be applied to obesity? • Does obesity represent an addiction to food? Lessons from tobacco • Smoking incidence – 90% after WWI – 15% today (California) • Effective Measures – Cost increase – Prohibition – Cue elimination – Behavioral Therapy – Replacement therapy (nicotine gum, patch) – Drugs acting on the reward system (Zyban, rimonabant) “Food addiction” Pro • Shared neural circuitry • Dopamine • Conceptual similairty • Shared risk factors – Genetic – Endophenotypes • Hints for effective treatments Con • Addiction has no formal definition • Drug addiction has a wide spectrum • Loaded term • Is “food addiction” really a cause of obesity?