title: Sucrose ingestion induces rapid AMPA receptor trafficking.
abstract: 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.
authors.affiliation: Department of Biochemistry and Molecular Pharmacology, New York, New York 10016, and Center for Neural Science, New York University, New York, New York 10003, USA.
authors.forename: David S
authors.initials: DS
authors.lastname: Tukey
authors.forename: Jainne M
authors.initials: JM
authors.lastname: Ferreira
authors.forename: Shannon O
authors.initials: SO
authors.lastname: Antoine
authors.forename: James A
authors.initials: JA
authors.lastname: D'amour
authors.forename: Ipe
authors.initials: I
authors.lastname: Ninan
authors.forename: Soledad
authors.initials: S
authors.lastname: Cabeza de Vaca
authors.forename: Salvatore
authors.initials: S
authors.lastname: Incontro
authors.forename: Charlotte
authors.initials: C
authors.lastname: Wincott
authors.forename: Julian K
authors.initials: JK
authors.lastname: Horwitz
authors.forename: Diana T
authors.initials: DT
authors.lastname: Hartner
authors.forename: Carlo B
authors.initials: CB
authors.lastname: Guarini
authors.forename: Latika
authors.initials: L
authors.lastname: Khatri
authors.forename: Yossef
authors.initials: Y
authors.lastname: Goffer
authors.forename: Duo
authors.initials: D
authors.lastname: Xu
authors.forename: Roseann F
authors.initials: RF
authors.lastname: Titcombe
authors.forename: Megna
authors.initials: M
authors.lastname: Khatri
authors.forename: Dave S
authors.initials: DS
authors.lastname: Marzan
authors.forename: Shahana S
authors.initials: SS
authors.lastname: Mahajan
authors.forename: Jing
authors.initials: J
authors.lastname: Wang
authors.forename: Robert C
authors.initials: RC
authors.lastname: Froemke
authors.forename: Kenneth D
authors.initials: KD
authors.lastname: Carr
authors.forename: Chiye
authors.initials: C
authors.lastname: Aoki
authors.forename: Edward B
authors.initials: EB
authors.lastname: Ziff
mesh_terms: D000818:Animals; D002352:Carrier Proteins; D003216:Conditioning, Operant / Q000502:physiology; D004299:Dopamine beta-Hydroxylase / Q000378:metabolism; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects; D066298:In Vitro Techniques; D008124:Locomotion / Q000502:physiology; D008297:Male; D046529:Microscopy, Electron, Transmission; D009474:Neurons / Q000187:drug effects / Q000378:metabolism*; D009714:Nucleus Accumbens / Q000166:cytology; D010750:Phosphoproteins / Q000378:metabolism; D057907:Post-Synaptic Density / Q000378:metabolism / Q000648:ultrastructure; D021381:Protein Transport / Q000187:drug effects; D051381:Rats; D017207:Rats, Sprague-Dawley; D018091:Receptors, AMPA / Q000378:metabolism*; D013347:Subcellular Fractions / Q000378:metabolism; D013395:Sucrose / Q000008:administration & dosage*; D013549:Sweetening Agents / Q000008:administration & dosage*; D013574:Synaptosomes / Q000378:metabolism / Q000648:ultrastructure
chemical_list: D002352:Carrier Proteins; D004299:Dopamine beta-Hydroxylase; D010750:Phosphoproteins; D018091:Receptors, AMPA; D013395:Sucrose; D013549:Sweetening Agents; C461219:RNF34 protein, human
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