Functional Connectivity Within the Gustatory Network Is Altered by Fat Content and Oral Fat Sensitivity – A Pilot Study

Background: The amount of fat in ingested food dictates specific activation patterns in the brain, particularly in homeostatic and reward-related areas. Taste-specific brain activation changes have also been shown and the sensitivity to the oral perception of fat is associated with differential eating behavior and physiological parameters. The association between oral fat sensitivity and neuronal network functions has, however, not yet been defined. Objective: We aimed to investigate the association between fat-dependent neuronal functional connectivity patterns and oral fat sensitivity. Design: To investigate the underlying changes in network dynamics caused by fat intake, we measured resting-state functional connectivity in 11 normal-weight male participants before and after a high- vs. a low-fat meal on two separate study days. Oral fat sensitivity was also measured on both days. We used a high-resolution functional magnetic resonance imaging (MRI) sequence to measure any connectivity changes in networks with the seed in the brainstem (nucleus tractus solitarii, NTS), in homeostatic (hypothalamus) and in reward regions (ventral and dorsal striatum). Seed-based functional connectivity (FC) maps were analyzed using factorial analyses and correlation analyses with oral fat sensitivity were also performed. Results: Regardless of fat content, FC between NTS and reward and gustatory areas was lower after ingestion. Oral fat sensitivity was positively correlated with FC between homeostatic regions and limbic areas in the high-fat condition, but negatively correlated with FC between the dorsal striatum and somatosensory regions in the low-fat condition. Conclusion: Our results show the interaction of oral fat sensitivity with the network based neuronal processing of high- vs. low-fat meals. Variations in neuronal connectivity network patterns might therefore be a possible moderator of the association of oral fat sensitivity and eating behavior.

[1]  D. Gabriel,et al.  Reliability of a simple method for determining muscle fiber conduction velocity , 2012, Muscle & nerve.

[2]  Sally Eldeghaidy,et al.  Prior Consumption of a Fat Meal in Healthy Adults Modulates the Brain’s Response to Fat123 , 2016, The Journal of nutrition.

[3]  R. Keast,et al.  Detection thresholds for four different fatty stimuli are associated with increased dietary intake of processed high-caloric food , 2018, Appetite.

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

[5]  R. Mattes.  Fat taste and lipid metabolism in humans , 2005, Physiology & Behavior.

[6]  H. Preissl,et al.  Controversies in fat perception , 2015, Physiology & Behavior.

[7]  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.

[8]  P. Clifton,et al.  Oral sensitivity to fatty acids, food consumption and BMI in human subjects , 2010, British Journal of Nutrition.

[9]  B. Everitt,et al.  Cocaine Seeking Habits Depend upon Dopamine-Dependent Serial Connectivity Linking the Ventral with the Dorsal Striatum , 2008, Neuron.

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

[11]  R. Keast,et al.  The Test–Retest Reliability of Fatty Acid Taste Thresholds , 2013, Chemosensory Perception.

[12]  R. Veit,et al.  Fat intake modulates cerebral blood flow in homeostatic and gustatory brain areas in humans. , 2012, The American journal of clinical nutrition.

[13]  A. Chun,et al.  On the brain , 2007, Nature Nanotechnology.

[14]  L. Barsalou,et al.  A core eating network and its modulations underlie diverse eating phenomena , 2016, Brain and Cognition.

[15]  L. Marciani,et al.  Effect of meal viscosity and nutrients on satiety, intragastric dilution, and emptying assessed by MRI. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[16]  Xi-Nian Zuo,et al.  REST: A Toolkit for Resting-State Functional Magnetic Resonance Imaging Data Processing , 2011, PloS one.

[17]  Osama Mawlawi,et al.  Imaging Human Mesolimbic Dopamine Transmission with Positron Emission Tomography: I. Accuracy and Precision of D2 Receptor Parameter Measurements in Ventral Striatum , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  Elizabeth Tricomi,et al.  Value and probability coding in a feedback-based learning task utilizing food rewards. , 2015, Journal of neurophysiology.

[19]  E. Rolls,et al.  How the brain represents the reward value of fat in the mouth. , 2010, Cerebral cortex.

[20]  Michael W. Schwartz,et al.  Neurobiology of food intake in health and disease , 2014, Nature Reviews Neuroscience.

[21]  P. Smeets,et al.  Empty calories and phantom fullness: a randomized trial studying the relative effects of energy density and viscosity on gastric emptying determined by MRI and satiety. , 2016, The American journal of clinical nutrition.

[22]  R. Mattes.  Fat Taste in Humans: Is It a Primary? , 2010 .

[23]  L. Davachi,et al.  Distortion and Signal Loss in Medial Temporal Lobe , 2009, PloS one.

[24]  Shantanu P. Jadhav,et al.  Interaction of Taste and Place Coding in the Hippocampus , 2018, The Journal of Neuroscience.

[25]  D. Hill,et al.  Development and Plasticity of the Gustatory Portion of Nucleus of the Solitary Tract , 2007 .

[26]  Moors Pieter,et al.  Test-retest reliability. , 2014 .

[27]  M. Bellon,et al.  Acute effects of oral preloads with increasing energy density on gastric emptying, gut hormone release, thermogenesis and energy intake, in overweight and obese men. , 2013, Asia Pacific journal of clinical nutrition.

[28]  M. Gallani,et al.  Reliability of a Simple Method for Determining Salt Taste Detection and Recognition Thresholds. , 2016, Chemical senses.

[29]  Remco J. Renken,et al.  Neural processing of basic tastes in healthy young and older adults — an fMRI study , 2015, NeuroImage.

[30]  B. Tuschen-Caffier,et al.  Eating Disorder Examination: Deutschsprachige Version des strukturierten Essstörungsinterviews , 2004 .

[31]  Dana M. Small,et al.  Taste representation in the human insula , 2010, Brain Structure and Function.

[32]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[33]  R. Keast,et al.  Oral sensitivity to oleic acid is associated with fat intake and body mass index. , 2011, Clinical nutrition.

[34]  A. Foundas,et al.  The Role of the Insular Cortex in Dysphagia , 1997, Dysphagia.

[35]  R. Veit,et al.  Dose-Dependent Effects of Intranasal Insulin on Resting-State Brain Activity , 2018, The Journal of clinical endocrinology and metabolism.

[36]  R. Keast,et al.  The influence of a high-fat meal on fat taste thresholds , 2016, Appetite.

[37]  J. Victor,et al.  Taste response variability and temporal coding in the nucleus of the solitary tract of the rat. , 2003, Journal of neurophysiology.

[38]  D. Carnall,et al.  Eating disorders , 1999, International Journal of Obesity.

[39]  R. Mattes.  Oral detection of short-, medium-, and long-chain free fatty acids in humans. , 2008, Chemical senses.

[40]  Yufeng Zang,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010 .

[41]  Fabian Grabenhorst,et al.  The representation of oral fat texture in the human somatosensory cortex , 2014, Human brain mapping.

[42]  R J Zatorre,et al.  Changes in taste intensity perception following anterior temporal lobe removal in humans. , 2001, Chemical senses.

[43]  R. Keast,et al.  Is fat the sixth taste primary? Evidence and implications , 2015, Flavour.

[44]  Miguel Macías Macías,et al.  Acetic Acid Detection Threshold in Synthetic Wine Samples of a Portable Electronic Nose , 2012, Sensors.

[45]  K. Scheffler,et al.  Fat label compared with fat content: gastrointestinal symptoms and brain activity in functional dyspepsia patients and healthy controls. , 2018, The American journal of clinical nutrition.

[46]  O. Contreras-Rodríguez,et al.  Ventral and Dorsal Striatum Networks in Obesity: Link to Food Craving and Weight Gain , 2017, Biological Psychiatry.

[47]  A. Dagher,et al.  The Use of Functional Magnetic Resonance Imaging in the Study of Appetite and Obesity , 2017 .

[48]  J. Hinrichs,et al.  Oil Perception—Detection Thresholds for Varying Fatty Stimuli and Inter-individual Differences , 2017, Chemical senses.

[49]  D. Piomelli,et al.  Intestinal lipid-derived signals that sense dietary fat. , 2015, The Journal of clinical investigation.

[50]  A. Molero-Chamizo,et al.  Effects of lesions in different nuclei of the amygdala on conditioned taste aversion , 2017, Experimental Brain Research.

[51]  R. Keast,et al.  Measuring Oral Fatty Acid Thresholds, Fat Perception, Fatty Food Liking, and Papillae Density in Humans , 2014, Journal of visualized experiments : JoVE.