Multiple Modes of Synaptic Excitation of Olfactory Bulb Granule Cells

Balu, Ramani; Pressler, R. Todd; Strowbridge, Ben W.

doi:10.1523/jneurosci.4630-06.2007

Cited by 161 publications

(202 citation statements)

References 54 publications

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“…There is a consensus that dendro-dendritic inhibition plays an important role in synchronization of the MCs (7,(17)(18)(19). However, the mechanisms for this synchronization are still controversial: the GCs are known to be able to spike and produce graded inhibition, and the roles of these two types of inhibition in synchronization are unknown.…”

Section: Discussionmentioning

confidence: 99%

“…There may be several ways of amplifying the excitability of GCDs via neuromodulatory inputs to the external plexiform layer, which may underlie enhancement of gamma oscillations in different cognitive circumstances. A recent study showed that cholinergic drive from M1 receptors on GCDs enhances excitability of GCDs and elevates intracellular Ca 2ϩ (19).…”

Section: Discussionmentioning

confidence: 99%

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Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations

Brea

Kay

Kopell

2009

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

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Gamma oscillations in the olfactory bulb can be produced as an interaction of subthreshold oscillations (STOs) in the mitral cells (MCs) with inhibitory granule cells (GCs). The mechanism does not require that the GCs spike, and we work in a regime in which the MCs fire at rates lower than the fast gamma rhythm they create. The frequency of the network is that of the STOs, allowing the gamma to be modulated in amplitude with only small changes in frequency. Gamma oscillations could also be obtained with spiking GCs, but only for GCs firing close to population rate. Our mechanism differs from the more standard description of the gamma oscillation, in which the the decay time of the inhibitory cells is critical to the frequency of the network.mitral cell ͉ granule cell ͉ graded inhibition G amma oscillations (40-100 Hz) are produced in the mammalian olfactory bulb (OB) and many other structures in the nervous system (1-3). In the neocortex and the hippocampus, gamma oscillations are believed to depend on fast-spiking interneurons, created either by the interaction of inhibitory cells alone or as an interaction of excitatory pyramidal cells and inhibitory interneurons, such as basket cells (4,5). It is generally accepted that interactions between excitatory mitral cells (MCs) and inhibitory granule cells (GCs) at the dendrodendritic reciprocal synapse support gamma oscillations in the OB, but the physiological mechanisms of these oscillations are not well understood. Many slice studies focus on regimes in which the axonless GCs spike. However, it has been suggested, by contrast, that gamma oscillations in the OB depend on the subtheshold oscillations (STOs) in MCs, the excitatory cells of the OB (6), and that spikes from the GCs, the inhibitory cells of the OB, may not play a major part in the gamma oscillation of the OB (ref. 7 and see also Discussion). It is not understood what differences these features might make in the mechanism of synchronization of the OB gamma rhythm.It is well known that a target population of cells can be synchronized by a common pulse of inhibition (5,8,9). The synchronization comes mainly from a shared suppression of firing until the inhibition has worn off sufficiently for the excitatory cells to fire. If the target cells are identical in drive, they will fire simultaneously; if they have somewhat different drives, they will fire with a small lag (5). With graded inhibition, it is less clear how the inhibition provides the synchronization: there is no clear decay time of inhibition, because the amplitude and time course of the inhibition is not stereotyped.Here, we show that the features of STOs and graded inhibition can work together to produce a mechanism for the synchronization of gamma. We are interested in the regime in which MCs, the excitatory cells of the OB, spike with a firing rate significantly below that of the population frequency, as seen experimentally (10). Unlike the classical excitation-inhibition of the pyramidal interneuron network gamma (PING), in which the decay t...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations

Brea

Kay

Kopell

2009

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

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“…S1 A and B) (4,25), and distal glutamatergic input synapses are colocalized with GABAergic output synapses in the distal domain with a 1:1 stoichiometry (7,24,26). PSD ϩ Cs in GCs were in tight apposition to the presynaptic marker bassoon in vivo (Fig.…”

Section: Development Of Glutamatergic Synaptic Input Sitesmentioning

confidence: 92%

“…It is possible that postnatal changes in the structure or function of axon terminals ending at GCs may result in different patterns of synaptic appearance in new GCs, and thus, could explain why axo-dendritic input does not develop before distal dendro-dendritic synapses in neonatal-generated GCs. However, axon terminals from the olfactory cortex ending at the GCs are already functional one week after birth (4,36), thus preceding the maturation of the neonatal-generated GCs that we studied. In addition, excitatory synapses in the proximal domain preceded those formed on the basal domain even though these two domains both receive axo-dendritic inputs.…”

Section: Influence Of Brain Maturation On Synapse Formation By New Nementioning

confidence: 97%

“…The apical dendrite can be divided into an unbranched segment emerging from the soma followed by a branched segment (distal domain). The basal dendrite (basal domain) and unbranched apical dendrite receive axo-dendritic glutamatergic input from axon collaterals of the OB's projection neurons and from the olfactory cortices (3)(4)(5)(6). The distal domain of the apical dendrite has bidirectional dendrodendritic synapses present in spines where input and output synapses are colocalized and functionally coupled.…”

mentioning

confidence: 99%

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Sequential development of synapses in dendritic domains during adult neurogenesis

Kelsch

Lin²,

Lois³

2008

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

127

178

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During the process of integration into brain circuits, new neurons develop both input and output synapses with their appropriate targets. The vast majority of neurons in the mammalian brain are generated before birth and integrate into immature circuits while these are being assembled. In contrast, adult-generated neurons face an additional challenge as they integrate into a mature, fully functional circuit. Here, we examined how synapses of a single neuronal type, the granule cell in the olfactory bulb, develop during their integration into the immature circuit of the newborn and the fully mature circuit of the adult rat. We used a genetic method to label pre and postsynaptic sites in granule neurons and observed a stereotypical development of synapses in specific dendritic domains. In adult-generated neurons, synapses appeared sequentially in different dendritic domains with glutamatergic input synapses that developed first at the proximal dendritic domain, followed several days later by the development of inputoutput synapses in the distal domain and additional input synapses in the basal domain. In contrast, for neurons generated in neonatal animals, input and input-output synapses appeared simultaneously in the proximal and distal domains, respectively, followed by the later appearance of input synapses to the basal domain. The sequential formation of synapses in adult-born neurons, with input synapses appearing before output synapses, may represent a cellular mechanism to minimize the disruption caused by the integration of new neurons into a mature circuit in the adult brain.bulb ͉ dendrite I ntegration of new neurons continues throughout life in the adult mammalian olfactory bulb (OB) (1, 2). During the process of integration into brain circuits, new neurons develop both input and output synapses with their appropriate targets. Whereas the majority of neurons in the olfactory bulb integrate into an immature circuit while it is being assembled, neurons generated in adulthood face an additional challenge as they integrate into a mature, fully functional circuit. In particular, the formation of synapses by a new neuron in a functioning circuit may interfere with circuit operation and, thus, it could result in maladaptive behaviors. Additionally, it is still not known whether new neurons integrating into the neonatal and adult olfactory system have the same or different functions in the circuit and, therefore, adult-and neonatal-generated neurons could employ different modes of integration. To compare how new neurons are added to neonatal and adult circuits, we examined the pattern of synapse development of a single neuronal type, the granule cell (GC) in the olfactory bulb, during its integration into the immature circuit of the newborn and the mature circuit of the adult rat.The majority of neurons added to the OB of adult rats are GC neurons. GCs are axonless inhibitory interneurons that have both a basal dendrite and an apical dendrite (Fig. 1A). The apical dendrite can be divided into an unbranched segm...

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Anatomy and Neurobiology of the Main and Accessory Olfactory Bulbs

Ennis

Holy

2015

Handbook of Olfaction and Gustation

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Multiple Modes of Synaptic Excitation of Olfactory Bulb Granule Cells

Cited by 161 publications

References 54 publications

Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations

Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations

Sequential development of synapses in dendritic domains during adult neurogenesis

Anatomy and Neurobiology of the Main and Accessory Olfactory Bulbs

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