Representation and transformation of sensory information in the mouse accessory olfactory system

In mice, nonvolatile social cues are detected and analyzed by the accessory olfactory system (AOS). Here we provide a first view of information processing in the AOS with respect to individual chemical cues. 12 sulfated steroids, recently discovered mouse AOS ligands, caused widespread activity among vomeronasal sensory neurons (VSNs), yet VSN responses clustered into a small number of repeated functional patterns or processing streams. Downstream neurons in the accessory olfactory bulb (AOB) responded to these ligands with enhanced signal/noise compared to VSNs. Although the dendritic connectivity of AOB mitral cells suggests the capacity for broad integration, most sulfated steroid responses were well-modeled by linear excitatory drive from just one VSN processing stream. However, a substantial minority demonstrated multi-stream integration. Most VSN excitation patterns were also observed in the AOB, but excitation by estradiol sulfate processing streams was rare, suggesting AOB circuit organization is specific to the biological relevance of sensed cues.

• Publication year

  2010

• Venue

  Nature Neuroscience

• Publication date

  2010-05-09

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1038/nn.2546PMID 20453853PMCID 2930753
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Sensing odorants and pheromones with chemosensory receptors.

  2009cited by this paper
• The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior.

  2009cited by this paper
• SR1, a Mouse Odorant Receptor with an Unusually Broad Response Profile

  2009cited by this paper
• Precision and diversity in an odor map on the olfactory bulb

  2009cited by this paper
• An ex vivo preparation of the intact mouse vomeronasal organ and accessory olfactory bulb.

  2009cited by this paper
• The accessory olfactory bulb in the adult rat: A cytological study of its cell types, neuropil, neuronal modules, and interactions with the main olfactory system

  2008cited by this paper
• Rat olfactory bulb mitral cells receive sparse glomerular inputs.

  2008cited by this paper
• Inhibition Shapes Sex Selectivity in the Mouse Accessory Olfactory Bulb

  2008cited by this paper
• Conditional genetic labeling of mitral cells of the mouse accessory olfactory bulb to visualize the organization of their apical dendritic tufts.

  2008cited by this paper
• Sulfated Steroids as Natural Ligands of Mouse Pheromone-Sensing Neurons

  2008cited by this paper
• Neural mechanisms underlying sex-specific behaviors in vertebrates.

  2007cited by this paper
• Firing properties of accessory olfactory bulb mitral/tufted cells in response to urine delivered to the vomeronasal organ of gray short-tailed opossums.

  2007cited by this paper
• Sparse and Selective Odor Coding by Mitral/Tufted Neurons in the Main Olfactory Bulb

  2007cited by this paper
• Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations

  2007cited by this paper
• A multireceptor genetic approach uncovers an ordered integration of VNO sensory inputs in the accessory olfactory bulb.

  2006cited by this paper
• A Mathematical Theory of Communication

  2006cited by this paper
• Coding of odors by a receptor repertoire.

  2006cited by this paper
• Recording spikes from a large fraction of the ganglion cells in a retinal patch

  2004cited by this paper
• Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish.

  2004cited by this paper
• Neurotechnique In Vivo Imaging of Neuronal Activity by Targeted Expression of a Genetically Encoded Probe in the Mouse

  2004cited by this paper
• Intensity versus identity coding in an olfactory system.

  2003cited by this paper
• Encoding Pheromonal Signals in the Accessory Olfactory Bulb of Behaving Mice

  2003cited by this paper
• Correspondence between odorant-evoked patterns of receptor neuron input and intrinsic optical signals in the mouse olfactory bulb.

  2003cited by this paper
• Olfactory Bulb Mitral-Tufted Cell Plasticity: Odorant-Specific Tuning Reflects Previous Odorant Exposure

  2003cited by this paper
• Mean Shift: A Robust Approach Toward Feature Space Analysis

  2002cited by this paper
• Multiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors

  2002cited by this paper
• A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb.

  2002cited by this paper
• Oscillations and Sparsening of Odor Representations in the Mushroom Body

  2002cited by this paper
• Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes

  2002cited by this paper
• Co-Expression of Putative Pheromone Receptors in the Sensory Neurons of the Vomeronasal Organ

  2001cited by this paper
• Characterizing the sparseness of neural codes

  2001cited by this paper
• Responses of vomeronasal neurons to natural stimuli.

  2000cited by this paper
• Olfactory Neurons Expressing Closely Linked and Homologous Odorant Receptor Genes Tend to Project Their Axons to Neighboring Glomeruli on the Olfactory Bulb

  1999cited by this paper
• A map of pheromone receptor activation in the mammalian brain.

  1999cited by this paper
• Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system.

  1999cited by this paper
• Histology of the Nervous System of Man and Vertebrates

  1997cited by this paper
• Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging.

  1997cited by this paper
• Amplifying role of convergence in olfactory system a comparative study of receptor cell and second-order neuron sensitivities.

  1989cited by this paper

• Divergent synaptic dynamics originate parallel pathways for computation and behavior in an olfactory circuit.

  2025cites this paper
• Molecular, cellular, and developmental organization of the mouse vomeronasal organ at single cell resolution

  2024cites this paper
• Molecular, Cellular, and Developmental Organization of the Mouse Vomeronasal organ at Single Cell Resolution

  2024influential citation
• Mammalian chemosensory bile acid detection supports species and gut microbiome evaluation

  2024cites this paper
• Evolution of Sensory Receptors

  2024cites this paper
• Divergent short-term plasticity creates parallel pathways for computation and behavior in an olfactory circuit

  2024cites this paper
• Stimulus-Induced Theta-Band LFP Oscillations Format Neuronal Representations of Social Chemosignals in the Mouse Accessory Olfactory Bulb

  2023cites this paper
• Stimulus-induced theta band LFP oscillations format spiking outputs in the mouse accessory olfactory bulb

  2023cites this paper
• Coding of pheromones by vomeronasal receptors

  2021cites this paper
• Neural circuit mechanisms that govern inter-male attack in mice

  2021cites this paper
• Wiring and information processing in the olfactory bulb of larval Xenopus laevis

  2020influential citation
• Physiology-forward identification of bile acid–sensitive vomeronasal receptors

  2020influential citation
• Functional evolution of vertebrate sensory receptors.

  2020cites this paper
• A new molecular risk pathway for postpartum mood disorders: clues from steroid sulfatase–deficient individuals

  2020cites this paper
• Distinct evolutionary trajectories of V1R clades across mouse species

  2019cites this paper
• Paradoxically Sparse Chemosensory Tuning in Broadly Integrating External Granule Cells in the Mouse Accessory Olfactory Bulb

  2019influential citation
• Brain Gene Expression in a Novel Mouse Model of Postpartum Mood Disorder

  2019cites this paper
• Interneuron Functional Diversity in the Mouse Accessory Olfactory Bulb

  2019cites this paper
• Maternal Experience-Dependent Cortical Plasticity in Mice Is Circuit- and Stimulus-Specific and Requires MECP2

  2019cites this paper
• Neural circuits regulating sexual behaviors via the olfactory system in mice.

  2019cites this paper
• Physiology-forward identification of bile acid sensitive vomeronasal receptors

  2019influential citation
• Title: Maternal experience-dependent cortical plasticity in mice is circuit- and stimulus-specific and requires MECP2

  2019cites this paper
• Limbic Neurons Shape Sex Recognition and Social Behavior in Sexually Naive Males.

  2019cites this paper
• Neural coding of sex-specific social information in the mouse brain.

  2018cites this paper
• Excreted Steroids in Vertebrate Social Communication

  2018influential citation
• Signal Detection and Coding in the Accessory Olfactory System

  2018cites this paper
• Sensory Adaptation to Chemical Cues by Vomeronasal Sensory Neurons

  2018cites this paper
• Voluntary urination control by brainstem neurons that relax the urethral sphincter

  2018cites this paper
• The Accessory Olfactory System: Innately Specialized or Microcosm of Mammalian Circuitry?

  2018cites this paper
• Experience-Dependent Plasticity in Accessory Olfactory Bulb Interneurons following Male–Male Social Interaction

  2017cites this paper
• Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice.

  2017cites this paper
• Neural mechanisms of social learning in the female mouse

  2017cites this paper
• Heterogeneous effects of norepinephrine on spontaneous and stimulus-driven activity in the male accessory olfactory bulb.

  2017influential citation
• 5.05 – Sex Differences in and Hormone Effects on Mammalian Pheromonal Communication

  2017cites this paper
• Title Experience-dependent plasticity in accessory olfactory bulb interneurons following male-male social interaction Abbreviated title Accessory olfactory bulb inhibitory plasticity

  2017cites this paper
• Experience-Dependent Plasticity Drives Individual Differences in Pheromone-Sensing Neurons.

  2016cites this paper
• Faecal bile acids are natural ligands of the mouse accessory olfactory system

  2016cites this paper
• Odorant Responses and Courtship Behaviors Influenced by at4 Neurons in Drosophila

  2016cites this paper
• Vomeronasal Receptors: V1Rs, V2Rs, and FPRs

  2016cites this paper
• Vomeronasal Transduction and Cell Signaling

  2016cites this paper
• The Murine Accessory Olfactory Bulb as a Model Chemosensory System: Experimental and Computational Analysis of Chemosensory Representations

  2016influential citation
• Specialized Chemosignaling that Generates Social and Survival Behavior in Mammals

  2016cites this paper
• The Vomeronasal Organ

  2015cites this paper
• Extracting Social Information from Chemosensory Cues: Consideration of Several Scenarios and Their Functional Implications

  2015influential citation
• The organic anion transporter (OAT) family: a systems biology perspective.

  2015cites this paper
• Tuning properties and dynamic range of type 1 vomeronasal receptors

  2015cites this paper
• Neural map formation and sensory coding in the vomeronasal system

  2015cites this paper
• Neural Computation and Neuromodulation Underlying Social Behavior.

  2015cites this paper
• Extracellular pH Regulates Excitability of Vomeronasal Sensory Neurons

  2015cites this paper
• Convergence, Divergence, and Reconvergence in a Feedforward Network Improves Neural Speed and Accuracy.

  2015cites this paper
• Dual processing of sulfated steroids in the olfactory system of an anuran amphibian

  2015cites this paper
• A Molecular Code for Identity in the Vomeronasal System.

  2015cites this paper
• Anatomy and Neurobiology of the Main and Accessory Olfactory Bulbs

  2015cites this paper
• Postsynaptic Odorant Concentration Dependent Inhibition Controls Temporal Properties of Spike Responses of Projection Neurons in the Moth Antennal Lobe

  2014cites this paper
• Innate and learned aspects of pheromone-mediated social behaviours

  2014influential citation
• Large-scale Cellular Imaging of Neuronal Activity: a Study of Neural Individuality and a Method for Imaging Mouse Cortex

  2014influential citation
• Odor and Pheromone Molecules, Receptors, and Behavioral Responses

  2014cites this paper
• Mammalian pheromones.

  2014influential citation
• Central Processing of Intraspecific Chemical Signals in Mice -- Neurobiology of Chemical Communication

  2014cites this paper
• Functional organization of glomerular maps in the mouse accessory olfactory bulb

  2014cites this paper
• Integrated action of pheromone signals in promoting courtship behavior in male mice

  2014cites this paper
• Odorant Concentration Differentiator for Intermittent Olfactory Signals

  2014cites this paper
• Ex vivo preparations of the intact vomeronasal organ and accessory olfactory bulb.

  2014cites this paper
• How neurogenesis finds its place in a hardwired sensory system

  2014influential citation
• Estradiol rapidly modulates odor responses in mouse vomeronasal sensory neurons.

  2014cites this paper
• Roles of sex and gonadal steroids in mammalian pheromonal communication.

  2013cites this paper
• Wake up and smell the conflict: odour signals in female competition

  2013cites this paper
• Kirrel3 is required for the coalescence of vomeronasal sensory neuron axons into glomeruli and for male-male aggression

  2013cites this paper
• Reliable Sex and Strain Discrimination in the Mouse Vomeronasal Organ and Accessory Olfactory Bulb

  2013cites this paper
• Concentration Coding in the Accessory Olfactory System

  2013influential citation
• Olfactory Wiring Logic in Amphibians Challenges the Basic Assumptions of the Unbranched Axon Concept

  2013cites this paper
• Neural control of sexually dimorphic behaviors.

  2013cites this paper
• NGL-2 Regulates Pathway-Specific Neurite Growth and Lamination, Synapse Formation, and Signal Transmission in the Retina

  2013cites this paper
• The neuroanatomical organization and chemosensory response characteristics of the olfactory bulb in the sea lamprey (Petromyzon marinus)

  2013cites this paper
• Robust Encoding of Stimulus Identity and Concentration in the Accessory Olfactory System

  2013influential citation
• Fast Neuronal Imaging using Objective Coupled Planar Illumination Microscopy

  2012influential citation
• From genes to social communication: molecular sensing by the vomeronasal organ.

  2012cites this paper
• Organization of Vomeronasal Sensory Coding Revealed by Fast Volumetric Calcium Imaging

  2012cites this paper
• Responses to sulfated steroids of female mouse vomeronasal sensory neurons.

  2012cites this paper
• Development, Organization and Plasticity of the Zebrafish Olfactory System

  2011cites this paper
• Chemosensory burst coding by mouse vomeronasal sensory neurons.

  2011influential citation
• Distinct intrinsic membrane properties determine differential information processing between main and accessory olfactory bulb mitral cells.

  2011influential citation
• Steroid catabolism in marine and freshwater fish.

  2011cites this paper
• Remote Communication through Solute Carriers and ATP Binding Cassette Drug Transporter Pathways: An Update on the Remote Sensing and Signaling Hypothesis

  2011cites this paper
• Sexually dimorphic effects of estrogen on spines in cultures of accessory olfactory bulb.

  2011cites this paper
• Sexual dimorphism in olfactory signaling.

  2010cites this paper