Olfactory mechanisms of stereotyped behavior: on the scent of specialized circuits

Investigation of how specialized olfactory cues, such as pheromones, are detected has primarily focused on the function of receptor neurons within a subsystem of the nasal cavity, the vomeronasal organ (VNO). Behavioral analyses have long indicated that additional, non-VNO olfactory neurons are similarly necessary for pheromone detection; however, the identity of these neurons has been a mystery. Recent molecular, behavioral, and genomic approaches have led to the identification of multiple atypical sensory circuits that display characteristics suggestive of a specialized function. This review focuses on these non-VNO receptors and neurons, and evaluates their potential for mediating stereotyped olfactory behavior in mammals.

[1]  Peter Mombaerts,et al.  Specificity of Glomerular Targeting by Olfactory Sensory Axons , 2002, The Journal of Neuroscience.

[2]  D. Storm,et al.  Pheromone Detection in Male Mice Depends on Signaling through the Type 3 Adenylyl Cyclase in the Main Olfactory Epithelium , 2006, The Journal of Neuroscience.

[3]  Janet M. Young,et al.  Degeneration of the Olfactory Guanylyl Cyclase D Gene during Primate Evolution , 2007, PloS one.

[4]  H. Innan,et al.  Relaxed selective pressure on an essential component of pheromone transduction in primate evolution , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Anna Menini,et al.  From pheromones to behavior. , 2009, Physiological reviews.

[6]  T. Holy,et al.  Loss of sex discrimination and male-male aggression in mice deficient for TRP2. , 2002, Nature Reviews Genetics.

[7]  J. Ngai,et al.  General Anosmia Caused by a Targeted Disruption of the Mouse Olfactory Cyclic Nucleotide–Gated Cation Channel , 1996, Neuron.

[8]  Martin H. Teicher,et al.  Suckling pheromone stimulation of a modified glomerular region in the developing rat olfactory bulb revealed by the 2-deoxyglucose method , 1980, Brain Research.

[9]  D. Logan,et al.  Species Specificity in Major Urinary Proteins by Parallel Evolution , 2008, PloS one.

[10]  S. Munger,et al.  Afferent activity to necklace glomeruli is dependent on external stimuli , 2009, BMC Research Notes.

[11]  T. Holy,et al.  Sex- and Strain-Specific Expression and Vomeronasal Activity of Mouse ESP Family Peptides , 2007, Current Biology.

[12]  C. Mucignat-Caretta,et al.  Time course of alterations after olfactory bulbectomy in mice , 2006, Physiology & Behavior.

[13]  R. Hudson,et al.  The contribution of the olfactory and tactile modalities to the nipple-search behaviour of newborn rabbits , 1985, Journal of Comparative Physiology A.

[14]  Martin H. Teicher,et al.  Functional development of the olfactory bulb and a unique glomerular complex in the neonatal rat , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  L. Vosshall,et al.  Genetic variation in a human odorant receptor alters odour perception , 2007, Nature.

[16]  P. Karlson,et al.  ‘Pheromones’: a New Term for a Class of Biologically Active Substances , 1959, Nature.

[17]  S. Korsching,et al.  Positive Darwinian selection and the birth of an olfactory receptor clade in teleosts , 2009, Proceedings of the National Academy of Sciences.

[18]  Susan C. Roberts,et al.  Evidence that androstadienone, a putative human chemosignal, modulates women’s attributions of men’s attractiveness , 2008, Hormones and Behavior.

[19]  Minmin Luo,et al.  Guanylyl cyclase-D in the olfactory CO2 neurons is activated by bicarbonate , 2009, Proceedings of the National Academy of Sciences.

[20]  L. Enquist,et al.  Olfactory Inputs to Hypothalamic Neurons Controlling Reproduction and Fertility , 2005, Cell.

[21]  R. Hudson,et al.  Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ , 1986, Physiology & Behavior.

[22]  S. Munger,et al.  Heterogeneous Sensory Innervation and Extensive Intrabulbar Connections of Olfactory Necklace Glomeruli , 2009, PloS one.

[23]  Xin-Yun Huang,et al.  Stimulation of guanylyl cyclase-D by bicarbonate. , 2009, Biochemistry.

[24]  N. Shah,et al.  Deficits in sexual and aggressive behaviors in Cnga2 mutant mice , 2005, Nature Neuroscience.

[25]  L. Buck,et al.  Feedback Loops Link Odor and Pheromone Signaling with Reproduction , 2005, Cell.

[26]  R. Axel,et al.  A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[27]  K. Shinoda,et al.  “Necklace olfactory glomeruli” form unique components of the rat primary olfactory system , 1989, The Journal of comparative neurology.

[28]  D. Juilfs,et al.  A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Itohara,et al.  Innate versus learned odour processing in the mouse olfactory bulb , 2007, Nature.

[30]  Linda B. Buck,et al.  A second class of chemosensory receptors in the olfactory epithelium , 2006, Nature.

[31]  Richard Axel,et al.  Mice with a “Monoclonal Nose”: Perturbations in an Olfactory Map Impair Odor Discrimination , 2008, Neuron.

[32]  A. Holley,et al.  Mammary olfactory signalisation in females and odor processing in neonates: Ways evolved by rabbits and humans , 2009, Behavioural Brain Research.

[33]  R. Khan,et al.  Smelling a Single Component of Male Sweat Alters Levels of Cortisol in Women , 2007, The Journal of Neuroscience.

[34]  P. Mombaerts,et al.  The Grueneberg ganglion of the mouse projects axons to glomeruli in the olfactory bulb , 2005, The European journal of neuroscience.

[35]  T. Holy,et al.  Sulfated Steroids as Natural Ligands of Mouse Pheromone-Sensing Neurons , 2008, The Journal of Neuroscience.

[36]  S. Fraser,et al.  Grueneberg ganglion olfactory subsystem employs a cGMP signaling pathway , 2009, The Journal of comparative neurology.

[37]  S. Liberles,et al.  Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ , 2009, Proceedings of the National Academy of Sciences.

[38]  H. Breer,et al.  Olfactory receptors and signalling elements in the Grueneberg ganglion , 2006, Journal of neurochemistry.

[39]  B. P. Halpern,et al.  Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. , 1997, Brain, behavior and evolution.

[40]  A. Saghatelian,et al.  Identification of protein pheromones that promote aggressive behaviour , 2007, Nature.

[41]  H. Grüneberg.  A ganglion probably belonging to the N. terminalis system in the nasal mucosa of the mouse , 1973, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[42]  H. Breer,et al.  Grueneberg ganglion neurons respond to cool ambient temperatures , 2008, The European journal of neuroscience.

[43]  Rameshwar K. Sharma,et al.  ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer. , 2008, Biochemical and biophysical research communications.

[44]  P. Sorensen,et al.  Isolation and Biological Activity of the Multi-Component Sea Lamprey Migratory Pheromone , 2008, Journal of Chemical Ecology.

[45]  F. Zufall,et al.  Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium , 2007, Proceedings of the National Academy of Sciences.

[46]  F. Zufall,et al.  Structural requirements for the activation of vomeronasal sensory neurons by MHC peptides , 2009, Nature Neuroscience.

[47]  Minmin Luo,et al.  Detection of Near-Atmospheric Concentrations of CO2 by an Olfactory Subsystem in the Mouse , 2007, Science.

[48]  S. Liberles,et al.  Trace Amine‐associated Receptors Are Olfactory Receptors in Vertebrates , 2009, Annals of the New York Academy of Sciences.

[49]  I. Rodriguez,et al.  Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors , 2009, Nature.

[50]  K. Touhara,et al.  Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons , 2005, Nature.

[51]  Mutsumi Nishida,et al.  Evolution of trace amine associated receptor (TAAR) gene family in vertebrates: lineage-specific expansions and degradations of a second class of vertebrate chemosensory receptors expressed in the olfactory epithelium. , 2007, Molecular biology and evolution.

[52]  C. Dulac,et al.  Molecular detection of pheromone signals in mammals: from genes to behaviour , 2003, Nature Reviews Neuroscience.

[53]  F. Zufall,et al.  Altered sexual and social behaviors in trp2 mutant mice , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[54]  H. Breer,et al.  Expression of cGMP signaling elements in the Grueneberg ganglion , 2008, Histochemistry and Cell Biology.

[55]  R. Hall,et al.  Olfactory receptor trafficking to the plasma membrane , 2008, Cellular and Molecular Life Sciences.

[56]  L. Stowers,et al.  What Is a Pheromone? Mammalian Pheromones Reconsidered , 2005, Neuron.

[57]  M. Broillet,et al.  Grueneberg Ganglion Cells Mediate Alarm Pheromone Detection in Mice , 2008, Science.

[58]  S. Fraser,et al.  The Grueneberg ganglion projects to the olfactory bulb , 2005, Neuroreport.