A Multireceptor Genetic Approach Uncovers an Ordered Integration of VNO Sensory Inputs in the Accessory Olfactory Bulb

Wagner, Shlomo; Gresser, Amy L.; Torello, A. Thomas; Dulac, Catherine

doi:10.1016/j.neuron.2006.04.033

Cited by 126 publications

(130 citation statements)

References 45 publications

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“…VNO neurons tend to increase their firing rate in response to either male urine or female urine, but rarely to both. No such overall segregation based on sex of the urine donor was observed in AOB, consistent with a role for at least some sensory integration in the AOB (Takami and Graziadei, 1990;Del Punta et al, 2002;Wagner et al, 2006;Yonekura and Yokoi, 2008;Meeks et al, 2010).…”

Section: Discussionmentioning

confidence: 57%

Reliable Sex and Strain Discrimination in the Mouse Vomeronasal Organ and Accessory Olfactory Bulb

Tolokh

Holy

2013

J. Neurosci.

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Animals modulate their courtship and territorial behaviors in response to olfactory cues produced by other animals. In rodents, detecting these cues is the primary role of the accessory olfactory system (AOS). We sought to systematically investigate the natural stimulus coding logic and robustness in neurons of the first two stages of accessory olfactory processing, the vomeronasal organ (VNO) and accessory olfactory bulb (AOB). We show that firing rate responses of just a few well-chosen mouse VNO or AOB neurons can be used to reliably encode both sex and strain of other mice from cues contained in urine. Additionally, we show that this population code can generalize to new concentrations of stimuli and appears to represent stimulus identity in terms of diverging paths in coding space. Together, the results indicate that firing rate code on the temporal order of seconds is sufficient for accurate classification of pheromonal patterns at different concentrations and may be used by AOS neural circuitry to discriminate among naturally occurring urine stimuli.

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Section: Discussionmentioning

confidence: 57%

Reliable Sex and Strain Discrimination in the Mouse Vomeronasal Organ and Accessory Olfactory Bulb

Tolokh

Holy

2013

J. Neurosci.

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“…In the main olfactory system, relatively simple glomerular maps are formed with OSNs expressing the same OR coalescing into an average of two conserved glomeruli per OB. By contrast, a greater complexity of glomerular innervation is observed in the AOS, where VSNs expressing the same VR can innervate up to 30 different glomeruli in spatially conserved regions of the AOB (Belluscio et al, 1999;Del Punta et al, 2002;Wagner et al, 2006). Within these conserved domains, glomeruli innervated by VSNs expressing different VRs are intermingled, suggesting that accurate coalescence of VSN axons may be particularly important for the formation of a glomerular map.…”

Section: Aob Glomerular Map and The Control Of Pheromonal Responsesmentioning

confidence: 99%

Kirrel3 is required for the coalescence of vomeronasal sensory neuron axons into glomeruli and for male-male aggression

et al. 2013

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SUMMARYThe accessory olfactory system controls social and sexual interactions in mice that are crucial for survival. Vomeronasal sensory neurons (VSNs) form synapses with dendrites of second order neurons in glomeruli of the accessory olfactory bulb (AOB). Axons of VSNs expressing the same vomeronasal receptor coalesce into multiple glomeruli within spatially conserved regions of the AOB. Here we examine the role of the Kirrel family of transmembrane proteins in the coalescence of VSN axons within the AOB. We find that Kirrel2 and Kirrel3 are differentially expressed in subpopulations of VSNs and that their expression is regulated by activity. Although Kirrel3 expression is not required for early axonal guidance events, such as fasciculation of the vomeronasal tract and segregation of apical and basal VSN axons in the AOB, it is necessary for proper coalescence of axons into glomeruli. Ablation of Kirrel3 expression results in disorganization of the glomerular layer of the posterior AOB and formation of fewer, larger glomeruli. Furthermore, Kirrel3 −/− mice display a loss of male-male aggression in a resident-intruder assay. Taken together, our results indicate that differential expression of Kirrels on vomeronasal axons generates a molecular code that dictates their proper coalescence into glomeruli within the AOB.

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“…The ϳ150,000 neurons of the VNO ) express ϳ300 different receptor types; consequently, many cells will be expressing the same receptor type in any given VNO. In the AOS, multiple VSNs expressing the same receptor type project to a limited number of glomeruli in the AOB (Belluscio et al 1999;Rodriguez et al 1999;Del Punta et al 2002;Wagner et al 2006), meaning that there exists significant pooling of similar inputs. This pooling may allow the system to obtain a more reliable signal by averaging across redundant information, as indeed has been observed when comparing VSN responses to those of AOB neurons (Meeks et al 2010).…”

Section: Implications Of Vsn Properties On the Coding And Measuring Omentioning

confidence: 99%

Chemosensory burst coding by mouse vomeronasal sensory neurons

Arnson

Holy

2011

Journal of Neurophysiology

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Arnson HA, Holy TE. Chemosensory burst coding by mouse vomeronasal sensory neurons. J Neurophysiol 106: 409 -420, 2011. First published April 27, 2011 doi:10.1152/jn.00108.2011.-The capabilities of any sensory system are ultimately constrained by the properties of the sensory neurons: the ability to detect and represent stimuli is limited by noise due to spontaneous activity, and optimal decoding in downstream circuitry must be matched to the nature of the encoding performed at the input. Here, we investigated the firing properties of sensory neurons in the accessory olfactory system, a distinct sensory system specialized for detection of socially relevant odors. Using multielectrode array recording, we observed that sensory neurons are spontaneously active and highly variable across time and trials and that this spontaneous activity limits the ability to distinguish sensory responses from noise. Sensory neuron activity tended to consist of bursts that maintained remarkably consistent statistics during both spontaneous activity and in response to stimulation with sulfated steroids. This, combined with pharmacological and genetic intervention in the signal transduction cascade, indicates that sensory transduction plays a role in shaping overall spontaneous activity. These findings indicate that as-yet unexplored characteristics of the sensory transduction cascade significantly constrain the representation of sensory information by vomeronasal neurons. accessory olfactory system; bursting; signal transduction A CENTRAL GOAL OF SENSORY neurobiology is to reveal how neurons encode information about the environment. This goal has many facets, including efforts to understand the nature of the stimulus [e.g., reviewed in Knutsen and Ahissar (2009) (Rieke et al. 1997;Berry et al. 1997;Shadlen and Newsome 1998). The ability to decode information about the natural environment is heavily influenced by neuronal "noise"; depending on the particular neurons and circuits, responses can be reliable at the level of single action potentials (Berry et al. 1997) or show sufficient variability that many spikes and/or large populations of neurons are required for accurate decoding (Shadlen and Newsome 1998).The accessory olfactory system (AOS) is a distinct chemical sense found in most tetrapods. This system is specialized to detect nonvolatile compounds used in social communication. Chemical stimuli are pumped into the vomeronasal organ (VNO), where vomeronasal sensory neurons (VSNs) that express individual receptor proteins from large families (Touhara and Vosshall 2009) encode the identity and concentration of ligands via their spiking activity. In the mouse, the AOS is an attractive system for exploring sensory coding and its functional relevance, in part because of the modest number of processing stages between sensory input and behavioral output (Halpern 1987). While physiological investigation of this sensory system is quite recent, there has been progress in identifying VSNs ligands and key components of the sensory transduc...

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A Multireceptor Genetic Approach Uncovers an Ordered Integration of VNO Sensory Inputs in the Accessory Olfactory Bulb

Cited by 126 publications

References 45 publications

Reliable Sex and Strain Discrimination in the Mouse Vomeronasal Organ and Accessory Olfactory Bulb

Reliable Sex and Strain Discrimination in the Mouse Vomeronasal Organ and Accessory Olfactory Bulb

Kirrel3 is required for the coalescence of vomeronasal sensory neuron axons into glomeruli and for male-male aggression

Chemosensory burst coding by mouse vomeronasal sensory neurons

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