Sucrose ingestion induces rapid AMPA receptor trafficking

The mechanisms by which natural rewards such as sugar affect synaptic transmission and behavior are largely unexplored. Here, we investigate regulation of nucleus accumbens synapses by sucrose intake. Previous studies have shown that AMPA receptor (AMPAR) trafficking is a major mechanism for regulat...

Full description

Saved in:

Bibliographic Details
Published in:	The Journal of neuroscience Vol. 33; no. 14; pp. 6123 - 6132
Main Authors:	Tukey, David S, Ferreira, Jainne M, Antoine, Shannon O, D'amour, James A, Ninan, Ipe, Cabeza de Vaca, Soledad, Incontro, Salvatore, Wincott, Charlotte, Horwitz, Julian K, Hartner, Diana T, Guarini, Carlo B, Khatri, Latika, Goffer, Yossef, Xu, Duo, Titcombe, Roseann F, Khatri, Megna, Marzan, Dave S, Mahajan, Shahana S, Wang, Jing, Froemke, Robert C, Carr, Kenneth D, Aoki, Chiye, Ziff, Edward B
Format:	Journal Article
Language:	English
Published:	United States Society for Neuroscience 03-04-2013
Subjects:	Animals Carrier Proteins Conditioning, Operant - physiology Dopamine beta-Hydroxylase - metabolism Excitatory Postsynaptic Potentials - drug effects In Vitro Techniques Locomotion - physiology Male Microscopy, Electron, Transmission Neurons - drug effects Neurons - metabolism Nucleus Accumbens - cytology Phosphoproteins - metabolism Post-Synaptic Density - metabolism Post-Synaptic Density - ultrastructure Protein Transport - drug effects Rats Rats, Sprague-Dawley Receptors, AMPA - metabolism Subcellular Fractions - metabolism Sucrose - administration & dosage Sweetening Agents - administration & dosage Synaptosomes - metabolism Synaptosomes - ultrastructure
Online Access:	Get full text
Tags:	Add Tag No Tags, Be the first to tag this record!

Description
Summary:	The mechanisms by which natural rewards such as sugar affect synaptic transmission and behavior are largely unexplored. Here, we investigate regulation of nucleus accumbens synapses by sucrose intake. Previous studies have shown that AMPA receptor (AMPAR) trafficking is a major mechanism for regulating synaptic strength, and that in vitro, trafficking of AMPARs containing the GluA1 subunit takes place by a two-step mechanism involving extrasynaptic and then synaptic receptor transport. We report that in rat, repeated daily ingestion of a 25% sucrose solution transiently elevated spontaneous locomotion and potentiated accumbens core synapses through incorporation of Ca(2+)-permeable AMPA receptors (CPARs), which are GluA1-containing, GluA2-lacking AMPARs. Electrophysiological, biochemical, and quantitative electron microscopy studies revealed that sucrose training (7 d) induced a stable (>24 h) intraspinous GluA1 population, and that in these rats a single sucrose stimulus rapidly (5 min) but transiently (<24 h) elevated GluA1 at extrasynaptic sites. CPARs and dopamine D1 receptors were required in vivo for elevated locomotion after sucrose ingestion. Significantly, a 7 d protocol of daily ingestion of a 3% solution of saccharin, a noncaloric sweetener, induced synaptic GluA1 similarly to 25% sucrose ingestion. These findings identify multistep GluA1 trafficking, previously described in vitro, as a mechanism for acute regulation of synaptic transmission in vivo by a natural orosensory reward. Trafficking is stimulated by a chemosensory pathway that is not dependent on the caloric value of sucrose.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 S. S. Mahajan's present address: Department of Health Sciences, Hunter College, City University of New York, New York, NY 10010. S. Incontro's present address: Departamento de Bioquímica, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain. J. M. Ferreira's present address: Laboratório de Farmacologia Bioquímica e Molecular, Instituto de Ciências Biomédicas, Sala J1–17 do Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro-UFRJ, Av. Carlos Chagas Filho, 373-CEP: 21941-912-Ilha do Fundão, Rio de Janeiro, Brazil. Author contributions: D.S.T., I.N., S.C.d.V., S.I., J.W., R.C.F., K.D.C., C.A., and E.B.Z. designed research; D.S.T., J.M.F., S.O.A., J.A.D., I.N., S.I., C.W., J.K.H., D.T.H., C.B.G., L.K., Y.G., D.X., R.F.T., D.J.M., and S.S.M. performed research; D.S.T., I.N., S.I., C.W., M.K., R.C.F., K.D.C., C.A., and E.B.Z. analyzed data; D.S.T., C.W., and E.B.Z. wrote the paper.
ISSN:	0270-6474 1529-2401 1529-2401
DOI:	10.1523/jneurosci.4806-12.2013