The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity
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Cellular and Molecular Life Sciences
REVIEW
The neuroscience of sugars in taste, gut‑reward, feeding circuits, and obesity Ranier Gutierrez1 · Esmeralda Fonseca1 · Sidney A. Simon2 Received: 2 October 2019 / Revised: 6 January 2020 / Accepted: 10 January 2020 © Springer Nature Switzerland AG 2020
Abstract Throughout the animal kingdom sucrose is one of the most palatable and preferred tastants. From an evolutionary perspective, this is not surprising as it is a primary source of energy. However, its overconsumption can result in obesity and an associated cornucopia of maladies, including type 2 diabetes and cardiovascular disease. Here we describe three physiological levels of processing sucrose that are involved in the decision to ingest it: the tongue, gut, and brain. The first section describes the peripheral cellular and molecular mechanisms of sweet taste identification that project to higher brain centers. We argue that stimulation of the tongue with sucrose triggers the formation of three distinct pathways that convey sensory attributes about its quality, palatability, and intensity that results in a perception of sweet taste. We also discuss the coding of sucrose throughout the gustatory pathway. The second section reviews how sucrose, and other palatable foods, interact with the gut–brain axis either through the hepatoportal system and/or vagal pathways in a manner that encodes both the rewarding and of nutritional value of foods. The third section reviews the homeostatic, hedonic, and aversive brain circuits involved in the control of food intake. Finally, we discuss evidence that overconsumption of sugars (or high fat diets) blunts taste perception, the post-ingestive nutritional reward value, and the circuits that control feeding in a manner that can lead to the development of obesity. Keywords Sugars · Sweetness · Hedonic taste value · Nutritional value · Gut-reward · AgRP · LHA GABA neurons · Obesity Abbreviations 5-HT 5-Hydroxytryptamine or serotonin AgRP Agouti-related protein aIC Anterior insular cortex ARC Arcuate nucleus of the hypothalamus ATD Amino-terminal domain BLA Basolateral amygdala BNST Bed nucleus of the stria terminalis CALHM1/3 Ca2+-activated and voltage-dependent Ca2+ homeostasis modulator 1/3 hetero-hexameric ion channel CCK Cholecystokinin Cdh4 Cadherin 4 CeA Central amygdala * Ranier Gutierrez [email protected] 1
Laboratory of Neurobiology of Appetite, Department of Pharmacology, CINVESTAV, 07360 Mexico City, Mexico
Department of Neurobiology, Duke University Medical Center, Durham, NC 27710, USA
2
ChR2 Channelrhodopsin-2 CN Cranial nerve CNS Central nervous system CRD Cystein-rich domain CT Chorda tympani DA Dopamine DAG Diacylglycerol DAT Dopamine transporter promotor DS Dorsal striatum EEC Enteroendocrine cells Egr2 Early growth response 2 ENaC Epithelial Na+ channel GG Geniculate ganglion GIP Glucose-dependent insulinotropic peptide GLP-1 Glucagon-like peptide-1 GPN Sensory branch of the glossopharyngeal nerve IC Insular cortex
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