Taoran Qu1, Wenfei Han2, Jingjing Niu3, Jenny Tong4, Ivan E de Araujo5. 1. Laboratory of Oral Biomedical Science and Translational Medicine, School of Stomatology, Tongji University, Shanghai, China; The John B Pierce Laboratory, New Haven, CT, USA. 2. The John B Pierce Laboratory, New Haven, CT, USA; Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA; Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA. 3. The John B Pierce Laboratory, New Haven, CT, USA; Department of Medicine, Duke University Medical Center, Durham, NC, USA. 4. Department of Medicine, Duke University Medical Center, Durham, NC, USA. 5. The John B Pierce Laboratory, New Haven, CT, USA; Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA; Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Department of Physiology, Yale University School of Arts and Sciences, New Haven, CT, USA. Electronic address: Ivan.deAraujo@mssm.edu.
Abstract
BACKGROUND AND AIM: In most species, including humans, food preference is primarily controlled by nutrient value. However, the gut-brain pathways involved in preference learning remain elusive. The aim of the present study, performed in C57BL6/J mice, was to characterize the roles in nutrient preference of two critical elements of gut-brain pathways, i.e. the duodenum and vagal gut innervation. METHODS: Adult wild-type C57BL6/J mice from a normal-weight cohort sustained one of the following three procedures: duodenal-jejunal bypass intestinal rerouting (DJB), total subdiaphragmatic vagotomy (SDV), or sham surgery. Mice were assessed in short-term two-bottle preference tests before and after 24 h s exposures to solutions containing one of glutamate, lipids, sodium, or glucose. RESULTS: DJB and SDV interfered in preference formation in a nutrient-specific manner: whereas normal preference learning for lipids and glutamate was disrupted by both DJB and SDV, these interventions did not alter the formation of preferences for glucose. Interestingly, sodium preferences were abrogated by DJB but not by SDV. CONCLUSIONS: Different macronutrients make use of distinct gut-brain pathways to influence food preferences, thereby mirroring nutrient-specific processes of food digestion. Specifically, whereas both vagal innervation and duodenal sensing appear critical for generating responses to fats and protein, glucose preferences recruit post-duodenal, vagal-independent pathways in pair with the control of glucose homeostasis. Overall, our data suggest that the physiological processes involved in digesting and absorbing fats, amino acids, and glucose overlap with those mediating learned preferences for each of these nutrients.
BACKGROUND AND AIM: In most species, including humans, food preference is primarily controlled by nutrient value. However, the gut-brain pathways involved in preference learning remain elusive. The aim of the present study, performed in C57BL6/J mice, was to characterize the roles in nutrient preference of two critical elements of gut-brain pathways, i.e. the duodenum and vagal gut innervation. METHODS: Adult wild-type C57BL6/J mice from a normal-weight cohort sustained one of the following three procedures: duodenal-jejunal bypass intestinal rerouting (DJB), total subdiaphragmatic vagotomy (SDV), or sham surgery. Mice were assessed in short-term two-bottle preference tests before and after 24 h s exposures to solutions containing one of glutamate, lipids, sodium, or glucose. RESULTS: DJB and SDV interfered in preference formation in a nutrient-specific manner: whereas normal preference learning for lipids and glutamate was disrupted by both DJB and SDV, these interventions did not alter the formation of preferences for glucose. Interestingly, sodium preferences were abrogated by DJB but not by SDV. CONCLUSIONS: Different macronutrients make use of distinct gut-brain pathways to influence food preferences, thereby mirroring nutrient-specific processes of food digestion. Specifically, whereas both vagal innervation and duodenal sensing appear critical for generating responses to fats and protein, glucose preferences recruit post-duodenal, vagal-independent pathways in pair with the control of glucose homeostasis. Overall, our data suggest that the physiological processes involved in digesting and absorbing fats, amino acids, and glucose overlap with those mediating learned preferences for each of these nutrients.
Authors: Danna M Breen; Brittany A Rasmussen; Andrea Kokorovic; Rennian Wang; Grace W C Cheung; Tony K T Lam Journal: Nat Med Date: 2012-06 Impact factor: 53.440
Authors: Albino J Oliveira-Maia; Craig D Roberts; Q David Walker; Brooke Luo; Cynthia Kuhn; Sidney A Simon; Miguel A L Nicolelis Journal: PLoS One Date: 2011-09-27 Impact factor: 3.240
Authors: MaryAnn Bohland; Aleksey V Matveyenko; Maziyar Saberi; Arshad M Khan; Alan G Watts; Casey M Donovan Journal: Diabetes Date: 2014-04-11 Impact factor: 9.461
Authors: Madhawi M Aldhwayan; Werd Al-Najim; Aruchuna Ruban; Michael Alan Glaysher; Brett Johnson; Navpreet Chhina; Georgios K Dimitriadis; Christina Gabriele Prechtl; Nicholas A Johnson; James Patrick Byrne; Anthony Peter Goldstone; Julian P Teare; Carel W Le Roux; Alexander Dimitri Miras Journal: Nutrients Date: 2022-05-20 Impact factor: 6.706
Authors: Ana B Fernandes; Joaquim Alves da Silva; Joana Almeida; Guohong Cui; Charles R Gerfen; Rui M Costa; Albino J Oliveira-Maia Journal: Neuron Date: 2020-04-06 Impact factor: 17.173
Authors: Hans-Rudolf Berthoud; Christopher D Morrison; Karen Ackroff; Anthony Sclafani Journal: Int J Obes (Lond) Date: 2021-07-06 Impact factor: 5.095