title: The receptor guanylyl cyclase type D (GC-D) ligand uroguanylin promotes the acquisition of food preferences in mice.
abstract: Rodents rely on olfactory stimuli to communicate information between conspecifics that is critical for health and survival. For example, rodents that detect a food odor simultaneously with the social odor carbon disulfide (CS(2)) will acquire a preference for that food. Disruption of the chemosensory transduction cascade in CS(2-)sensitive olfactory sensory neurons (OSNs) that express the receptor guanylyl cyclase type D (GC-D; GC-D+ OSNs) will prevent mice from acquiring these preferences. GC-D+ OSNs also respond to the natriuretic peptide uroguanylin, which is excreted into urine and feces. We analyzed if uroguanylin could also act as a social stimulus to promote the acquisition of food preferences. We found that feces of mice that had eaten odored food, but not unodored food, promoted a strong preference for that food in mice exposed to the feces. Olfactory exploration of uroguanylin presented with a food odor similarly produced a preference that was absent when mice were exposed to the food odor alone. Finally, the acquisition of this preference was dependent on GC-D+ OSNs, as mice lacking GC-D (Gucy2d(-)(/-) mice) showed no preference for the demonstrated food. Together with our previous findings, these results demonstrate that the diverse activators of GC-D+ OSNs elicit a common behavioral result and suggest that this specialized olfactory subsystem acts as a labeled line for a type of associative olfactory learning.
authors.affiliation: Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, MD 21201, USA.
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Arakawa
authors.forename: Kevin R
authors.initials: KR
authors.lastname: Kelliher
authors.forename: Frank
authors.initials: F
authors.lastname: Zufall
authors.forename: Steven D
authors.initials: SD
authors.lastname: Munger
mesh_terms: D000818:Animals; D005518:Food Preferences / Q000187:drug effects*; D006162:Guanylate Cyclase / Q000172:deficiency / Q000378:metabolism*; D008024:Ligands; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D018345:Mice, Knockout; D045265:Natriuretic Peptides / Q000494:pharmacology*; D018034:Olfactory Receptor Neurons / Q000187:drug effects* / Q000201:enzymology / Q000378:metabolism; D011956:Receptors, Cell Surface / Q000172:deficiency / Q000378:metabolism*
chemical_list: D008024:Ligands; D045265:Natriuretic Peptides; D011956:Receptors, Cell Surface; C084362:uroguanylin; D006162:Guanylate Cyclase; C484774:Gucy2d protein, mouse
keywords: natriuretic peptide; olfaction; olfactory subsystem; social learning
references.citation: J Clin Invest. 2011 Sep;121(9):3384-6
references.pmid: 21865649
references.citation: J Comp Physiol Psychol. 1976 Aug;90(8):727-39
references.pmid: 987073
references.citation: J Comp Psychol. 1983 Dec;97(4):358-63
references.pmid: 6317281
references.citation: J Neurosci. 2006 Feb 15;26(7):1961-70
references.pmid: 16481428
references.citation: Nature. 2011 Sep 21;478(7368):241-5
references.pmid: 21937988
references.citation: Behav Brain Res. 2012 Jun 1;231(2):266-71
references.pmid: 21802448
references.citation: Mol Cell Biochem. 2010 Jan;334(1-2):191-7
references.pmid: 19941039
references.citation: Nature. 2010 Jul 1;466(7302):118-22
references.pmid: 20596023
references.citation: BMC Biol. 2010 Jun 03;8:75
references.pmid: 20525243
references.citation: Brain Pathol. 2007 Oct;17(4):448-59
references.pmid: 17919130
references.citation: Pharmacol Ther. 2004 Nov;104(2):137-62
references.pmid: 15518884
references.citation: Biochem Biophys Res Commun. 2008 Mar 7;367(2):440-5
references.pmid: 18178149
references.citation: Dev Psychobiol. 1987 Mar;20(2):209-15
references.pmid: 3582781
references.citation: Behav Brain Res. 2008 Nov 21;193(2):235-42
references.pmid: 18586054
references.citation: Annu Rev Physiol. 2009;71:115-40
references.pmid: 18808328
references.citation: Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14507-12
references.pmid: 17724338
references.citation: J Chem Ecol. 2001 Oct;27(10):1953-61
references.pmid: 11710604
references.citation: Nat Commun. 2013;4:1616
references.pmid: 23511480
references.citation: Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):11235-40
references.pmid: 21690383
references.citation: Cell. 2010 May 14;141(4):692-703
references.pmid: 20478258
references.citation: Science. 2007 Aug 17;317(5840):953-7
references.pmid: 17702944
references.citation: Physiol Behav. 1988;42(2):119-24
references.pmid: 3368530
references.citation: Ann N Y Acad Sci. 1985;443:203-15
references.pmid: 2990282
references.citation: J Neurosci. 2012 Jun 6;32(23):7907-16
references.pmid: 22674266
references.citation: Science. 2004 Nov 5;306(5698):1033-7
references.pmid: 15528444
references.citation: Nature. 2007 Dec 6;450(7171):899-902
references.pmid: 18064011
references.citation: J Clin Invest. 2011 Sep;121(9):3578-88
references.pmid: 21865642
references.citation: Curr Biol. 2010 Aug 24;20(16):1438-44
references.pmid: 20637621