Spontaneous Neural Activity Is Required for the Establishment and Maintenance of the Olfactory Sensory Map

Yu, Chong; Power, Jennifer; Barnea, Gilad; O’Donnell, Sean; Brown, Henry Phelps; Osborne, Joseph R.; Axel, Richard; Gogos, Joseph A.

doi:10.1016/s0896-6273(04)00224-7

Cited by 382 publications

(472 citation statements)

References 62 publications

(2 reference statements)

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“…Certainly action potential spike generation in olfactory sensory neurons that is propagated to mapped central targets is both shaped by chemical (odorant) evoked activity and modulated by voltage-gated activity (Yu et al, 2004). This is the first report demonstrating that centrally derived, voltage-gated activity alters refinement of connections to central targets and simultaneously reduces peripheral OSNs.…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 85%

“…NIH-PA Author Manuscript NIH-PA Author Manuscript dimensional map of receptor activation to provide the neural code to discriminate olfactory sensory information (Yu et al, 2004). Odorant quality is thus encoded by a specific combination of activated glomeruli (Mori et al, 1999;Strotmann et al, 2000), and the formation of glomeruli depends on contextual sorting of axons expressing like OR proteins (Belluscio et al, 2002;Mombaerts, 2006).…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

“…In their study, elimination of synaptic contacts did not cause axons within previously established glomeruli to wander, rather, new P2 axons coalesced at inappropriate locations and formed smaller glomeruli. Thus our results and those of Ardiles et al (2007) provide support for the notion that OB map stability and its continual refinement relies on a normal distribution or function of synaptic targets, such as mitral cell neurons, in the olfactory bulb.Axel and co-workers (Yu et al, 2004) suggest that spontaneous neural activity but not odorevoked activity is required for both the maintenance and precise connectivity inherent in the …”

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confidence: 99%

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Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

Biju

Marks

Mast

et al. 2007

J of Comparative Neurology

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Olfactory sensory neurons (OSNs) expressing a specific odorant receptor (OR) gene send axonal projections to specific glomeruli, creating a stereotypic olfactory sensory map. Odorant receptor sequence, G-protein cAMP signaling, and axon guidance molecules have been shown to direct axons of OSNs toward central targets in the olfactory bulb (OB). Although the OR sequence may act as one determinant, our objective was to elucidate the extent by which voltage-dependent activity of postsynaptic projection neurons in the OB centrally influences peripheral development and target destination of OSNs. We bred OR-tagged transgenic mice to homozygosity with mice that had a gene-targeted deletion of the Shaker potassium ion channel (Kv1.3) to elucidate how activity modulates synaptic connections that formulate the sensory map. Here we report that the Kv1.3 ion channel, which is predominantly expressed in mitral cells and whose gene-targeted deletion causes a "super-smeller" phenotype, alters synaptic refinement of axonal projections from OSNs expressing P2, M72, and MOR28 ORs. Absence of Kv1.3 voltage-gated activity caused the formation of small, heterogeneous, and supernumerary glomeruli that failed to undergo neural pruning over development. These changes were accompanied by a significant decrease in the number of P2-, M72-, and MOR28-expressing OSNs, which contained an overexpression of OR protein and G-protein G olf in the cilia of the olfactory epithelium. These findings suggest that voltage-gated activity of projection neurons is essential to refine primary olfactory projections and that it regulates proper expression of the transduction machinery at the periphery. Indexing termsolfactory coding; axon targeting; olfaction; odorant receptor; Kv1.3The development of precise connectivity and maintenance of an olfactory sensory map is thought to rely upon guidance molecules that are recognized by receptors on olfactory sensory neurons (OSNs) or that are regulated by G-protein-mediated cAMP signals (Bozza et al., 2002;St John et al., 2002;Imai et al., 2006; Lattermann et al., 2007;Sweeney et al., 2007). OSNs expressing a given olfactory receptor are primarily randomly dispersed within one of four zones in the main olfactory epithelium (Ressler et al., 1993;Vassar et al., 1993;Mombaerts et al., 1996) but send their axonal projections to spatially conserved glomeruli within the olfactory bulb (Mombaerts, 1996;Wang et al., 1998;Tsuboi et al., 1999). Thus the olfactory bulb (OB) serves as a two- NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript dimensional map of receptor activation to provide the neural code to discriminate olfactory sensory information (Yu et al., 2004). Odorant quality is thus encoded by a specific combination of activated glomeruli (Mori et al., 1999;Strotmann et al., 2000), and the formation of glomeruli depends on contextual sorting of axons expressing like OR proteins (Belluscio et al., 2002;Mombaerts, 2006).If contextual cues from adjacent homotypic interactions initiate...

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Section: Nih-pa Author Manuscriptmentioning

confidence: 85%

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

mentioning

confidence: 99%

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Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

Biju

Marks

Mast

et al. 2007

J of Comparative Neurology

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“…The conditional removal of distinct neuronal lineages will be advantageous in modeling and understanding human neurological disorders using mice as a model. Finally, to determine the impact a neural cell has on animal behavior, neural activity blockers could be expressed from cellular phenotyping alleles (Yu et al, 2004). For these alleles, it will be necessary to express the blockers in an inducible manner from the population of cells marked with GIFM.…”

Section: Future Prospects For Using Gifm To Analyze Cell Morphology mentioning

confidence: 99%

Genetic inducible fate mapping in mouse: Establishing genetic lineages and defining genetic neuroanatomy in the nervous system

Joyner

Zervas

2006

Developmental Dynamics

172

167

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A fascinating aspect of developmental biology is how organs are assembled in three dimensions over time. Fundamental to understanding organogenesis is the ability to determine when and where specific cell types are generated, the lineage of each cell, and how cells move to reside in their final position. Numerous methods have been developed to mark and follow the fate of cells in various model organisms used by developmental biologists, but most are not readily applicable to mouse embryos in utero because they involve physical marking of cells through injection of tracers. The advent of sophisticated transgenic and gene targeting techniques, combined with the use of site-specific recombinases, has revolutionized fate mapping studies in mouse. Furthermore, using genetic fate mapping to mark cells has opened up the possibility of addressing fundamental questions that cannot be studied with traditional methods of fate mapping in other organisms. Specifically, genetic fate mapping allows both the relationship between embryonic gene expression and cell fate (genetic lineage) to be determined, as well as the link between gene expression domains and anatomy (genetic anatomy) to be established. In this review, we present the ever-evolving development of genetic fate mapping techniques in mouse, especially the recent advance of Genetic Inducible Fate Mapping. We then review recent studies in the nervous system (focusing on the anterior hindbrain) as well as in the limb and with adult stem cells to highlight fundamental developmental processes that can be discovered using genetic fate mapping approaches. We end with a look toward the future at a powerful new approach that combines genetic fate mapping with cellular phenotyping alleles to study cell morphology, physiology, and function using examples from the nervous system. Developmental Dynamics 235:2376 -2385, 2006.

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“…Interestingly, the chance for observing coexpression decreases nearly ten times from newborns to young adults. We then asked whether such decrement depends on sensory experience, because survival of individual OSNs depends on the neuronal activity (Watt et al, 2004;Yu et al, 2004;Zhao and Reed, 2001). We performed unilateral naris closure on the newborn mice, and the coexpression frequency observed four weeks later was significantly higher than the untreated mice at the same age.…”

Section: Introductionmentioning

confidence: 99%

Activity plays a role in eliminating olfactory sensory neurons expressing multiple odorant receptors in the mouse septal organ

Tian

2008

Molecular and Cellular Neuroscience

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A fundamental belief in the field of olfaction is that each olfactory sensory neuron (OSN) expresses only one odorant receptor (OR) type. Here we report that coexpression of multiple receptors in single neurons does occur at a low frequency. This was tested by double in situ hybridization in the septal organ in which greater than 90% of the sensory neurons express one of nine identified ORs. Notably, the coexpression frequency is nearly ten times higher in newborn than in young adult mice, suggesting a reduction of the sensory neurons with multiple ORs during postnatal development. In addition, such reduction is prevented by four-week sensory deprivation or impaired apoptosis. Furthermore, the high coexpression frequency is restored following four-week naris closure performed in young adult mice. The results indicate that activity induced by sensory inputs plays a role in ensuring the one cell-one receptor rule in a subset of olfactory sensory neurons.

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Spontaneous Neural Activity Is Required for the Establishment and Maintenance of the Olfactory Sensory Map

Cited by 382 publications

References 62 publications

Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

Genetic inducible fate mapping in mouse: Establishing genetic lineages and defining genetic neuroanatomy in the nervous system

Activity plays a role in eliminating olfactory sensory neurons expressing multiple odorant receptors in the mouse septal organ

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