Centre–surround inhibition among olfactory bulb glomeruli

Aungst, Jason; Heyward, Philip M.; Puché, Adam C.; Karnup, Sergei; Hayar, Abdallah; Szabó, Gábor; Shipley, Michael T.

doi:10.1038/nature02185

Cited by 388 publications

(450 citation statements)

References 45 publications

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“…Because sensory neuron axons synapse directly onto M͞T dendrites (27) and JGNs shape the electrophysiological input from olfactory sensory neurons (12,28,29), JGN neurogenesis may play a role in maintaining correct wiring. Newly formed dendrites from newly arrived JGNs may provide the appropriate postsynaptic substrate for the in-growing axons of newly generated sensory neurons.…”

Section: Discussionmentioning

confidence: 99%

In vivo imaging of juxtaglomerular neuron turnover in the mouse olfactory bulb

Mizrahi

Lü

Irving

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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As a consequence of adult neurogenesis, the olfactory bulb (OB) receives a continuous influx of newborn neurons well into adulthood. However, their rates of generation and turnover, the factors controlling their survival, and how newborn neurons intercalate into adult circuits are largely unknown. To visualize the dynamics of adult neurogenesis, we produced a line of transgenic mice expressing GFP in Ϸ70% of juxtaglomerular neurons (JGNs), a population that undergoes adult neurogenesis. Using in vivo twophoton microscopy, time-lapse analysis of identified JGN cell bodies revealed a neuronal turnover rate of Ϸ3% of this population per month. Although new neurons appeared and older ones disappeared, the overall number of JGNs remained constant. This approach provides a dynamic view of the actual appearance and disappearance of newborn neurons in the vertebrate central nervous system, and provides an experimental substrate for functional analysis of adult neurogenesis.neurogenesis ͉ olfaction N ewborn neurons in the adult mammalian brain continuously migrate into the hippocampus and the olfactory bulb (OB) (1, 2). In the OB, newborn neurons originate in the subventricular zone and differentiate into two distinct populations of interneurons: granule cells and juxtaglomerular neurons (JGNs). Adult neurogenesis in the mammalian brain was discovered and has been primarily analyzed by methods that label dividing cells by incorporation of labeled cyclic nucleotides, such as radiolabeled thymidine or the uridine analogue 5-bromo-2-deoxyuridine (BrdUrd). These methods have significant limitations. For example, neither radiolabeled thymidine nor BrdUrd are neuron-specific, and both can be analyzed only in fixed tissue after histological processing. These caveats and others (see discussions in refs. 3 and 4) limit direct analysis of the dynamics of neurogenesis, such as turnover rates and subtle changes in levels of neurogenesis in response to different experimental conditions and manipulations.To study adult neurogenesis using an alternative approach, we developed transgenic mice expressing GFP in a subset of JGNs and imaged adult neurogenesis over periods of up to 3 months, in vivo. We observed an Ϸ3%-per-month turnover rate of JGN in the OB. The number of newly appearing JGNs (representing newborn neurons) was balanced by the number of JGNs disappearing (presumably by cell death) thereby maintaining a stable population of JGN neurons. ResultsLabeling of JGNs in Transgenic Mice. Using a methodology based on transgenic GFP expression under control of the Thy-1 promoter, Feng et al. (5) created a bevy of mouse lines in which distinct neuronal subpopulations were strongly labeled by GFP and other fluorescent proteins. These lines have proven invaluable for numerous in vivo imaging experiments (6-10) enabling visualization of axonal and dendritic dynamics in developing and adult animals. However, none of the existing lines of Thy-1-XFP mice has labeling in the regenerating populations of the OB (granule and juxtaglomerular neu...

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Section: Discussionmentioning

confidence: 99%

In vivo imaging of juxtaglomerular neuron turnover in the mouse olfactory bulb

Mizrahi

Lü

Irving

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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“…The nasal cavity, the olfactory epithelium and the olfactory bulb with its precisely organized glomeruli (Belluscio et al 2002;Aungst et al 2003) can be considered a functional whole, a sense organ, in analogy with the eye, which includes an optical part and a retina consisting of a photoreceptor layer connected to a complex neuronal circuitry. Here, we focus on the size of the olfactory organ.…”

Section: Introductionmentioning

confidence: 99%

Scaling of mammalian ethmoid bones can predict olfactory organ size and performance

Pihlström

Hemilä

Forsman³

et al. 2005

Proc. R. Soc. B.

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The relation between size and performance is central for understanding the evolution of sensory systems, and much interest has been focused on mammalian eyes and ears. However, we know very little about olfactory organ size (OOS), as data for a representative set of mammals are lacking. Here, we present a cranial endocast method for estimating OOS by measuring an easily accessible part of the system, the perforated part of the ethmoid bone, through which the primary olfactory axons reach the olfactory bulb. In 16 species, for which relevant data are available, the area of the perforated ethmoid bone is directly proportional to the area of the olfactory epithelium. Thus, the ethmoid bone is a useful indicator enabling us to analyse 150 species, and describe the distribution of OOS within the class Mammalia. In the future, a method using skull material may be applied to fossil skulls. In relation to skull size, humans, apes and monkeys have small olfactory organs, while prosimians have OOSs typical for mammals of their size. Large ungulates have impressive olfactory organs. Relating anatomy to published thresholds, we find that sensitivity increases with increasing absolute organ size.

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“…Identification of ET cells was based on a combination of morphological and physiological criteria established in previous studies (Pinching and Powell, 1971;Aungst et al, 2003;Hayar et al, 2004a). The ET cells tend to be distributed along the lower half of the glomeruli and their somata have larger diameters than periglomerular cells.…”

Section: Olfactory Nerve Stimulation Activates a Polyamine-sensitive mentioning

confidence: 99%

“…They encapsulate a dense tangle of dendrodendritic microcircuitry originating from a surrounding shell of diverse inhibitory interneurons, including several types of periglomerular cells and short axon cells. During odor information processing, these interneurons can mediate both recurrent inhibition in the same glomerulus (Murphy et al, 2005), and lateral inhibition between different glomeruli (Aungst et al, 2003).Another major element of the glomerular circuitry is a specialized class of principal neurons, the external tufted (ET) cells. Dendritic tufts of ET cells arborize extensively inside glomeruli, where they receive monosynaptic glutamatergic input from olfactory nerve terminals (Hayar et al, 2004a).…”

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confidence: 99%

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Calcium permeable AMPA receptors and autoreceptors in external tufted cells of rat olfactory bulb

Lowe

2007

Neuroscience

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Glomeruli are functional units of the olfactory bulb responsible for early processing of odor information encoded by single olfactory receptor genes. Glomerular neural circuitry includes numerous external tufted (ET) cells whose rhythmic burst firing may mediate synchronization of bulbar activity with the inhalation cycle. Bursting is entrained by glutamatergic input from olfactory nerve terminals, so specific properties of ionotropic glutamate receptors on ET cells are likely to be important determinants of olfactory processing. Particularly intriguing is recent evidence that α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptors of juxta-glomerular neurons may permeate calcium. This could provide a novel pathway for regulating ET cell signaling. We tested the hypothesis that ET cells express functional calcium-permeable AMPA receptors. In rat olfactory bulb slices, excitatory postsynaptic currents (EPSCs) in ET cells were evoked by olfactory nerve shock, and by uncaging glutamate. We found attenuation of AMPA/kainate EPSCs by 1-naphthyl acetyl-spermine (NAS), an open-channel blocker specific for calcium permeable AMPA receptors. Cyclothiazide strongly potentiated EPSCs, indicating a major contribution from AMPA receptors. The current-voltage (I-V) relation of uncaging EPSCs showed weak inward rectification which was lost after > ~ 10 min of whole-cell dialysis, and was absent in NAS. In kainatestimulated slices, Co 2+ ions permeated cells of the glomerular layer. Large AMPA EPSCs were accompanied by fluorescence signals in fluo-4 loaded cells, suggesting calcium permeation. Depolarizing pulses evoked slow tail currents with pharmacology consistent with involvement of calcium permeable AMPA autoreceptors. Tail currents were abolished by Cd 2+ and NBQX, and were sensitive to NAS block. Glutamate autoreceptors were confirmed by uncaging intracellular calcium to evoke a large inward current. Our results provide evidence that calcium permeable AMPA receptors reside on ET cells, and are divided into at least two functionally distinct pools -postsynaptic receptors at olfactory nerve synaptic terminals, and autoreceptors sensitive to glutamate released from dendrodendritic synapses. Keywordsglutamate; glomerulus; dendrite; uncaging; fluorescence; rectification Olfaction begins with the binding of odorants to olfactory receptors which transduce sensory input into action potentials in axons of the olfactory nerve. Axons of cells expressing the same receptor gene converge to stereotypic glomeruli in the superficial layer of the olfactory bulb, forming a topographic neural map of receptor activation (Mombaerts et al., 1996). The olfactory nerve terminals make direct excitatory synapses on dendrites of bulb output neurons, Address correspondence to: Dr. Graeme Lowe, Monell Chemical Senses Center, 3500 Market St, Philadelphia, PA 19104-3308, phone: 215-573-5110, fax: 215-898-2084, email: loweg@monell.org. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for ...

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Centre–surround inhibition among olfactory bulb glomeruli

Cited by 388 publications

References 45 publications

In vivo imaging of juxtaglomerular neuron turnover in the mouse olfactory bulb

In vivo imaging of juxtaglomerular neuron turnover in the mouse olfactory bulb

Scaling of mammalian ethmoid bones can predict olfactory organ size and performance

Calcium permeable AMPA receptors and autoreceptors in external tufted cells of rat olfactory bulb

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