Branch-Specific Ca<sup>2+</sup>Influx from Na<sup>+</sup>-Dependent Dendritic Spikes in Olfactory Granule Cells

Zelles, Tibor; Boyd, Jeffrey E.; Hardy, Alexandre B.; Delaney, Kerry R.

doi:10.1523/jneurosci.1419-05.2006

Cited by 56 publications

(53 citation statements)

References 36 publications

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“…3), we reasoned that granule cells are likely to be the major cell type contributing to the large increase in miniature IPSCs observed in our experiments. In addition, the persistence of DHPG-evoked spontaneous IPSCs in the presence of TTX, but their elimination by blockers of VGCCs, is consistent with studies in granule cells demonstrating that local or global calcium spikes are potential triggers of transmitter release (Egger et al, 2003(Egger et al, , 2005Midtgaard, 2003, 2005;Zelles et al, 2006). Thus, one possible mechanism for the action of DHPG is via direct depolarization of granule cells.…”

Section: Mechanisms Of Mglur1 Action In Granule Cellssupporting

confidence: 82%

Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors

Castro¹,

Hovis²,

Urban³

2007

J. Neurosci.

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Metabotropic glutamate receptors (mGluRs) modulate neural excitability and network tone in many brain regions. Expression of mGluRs is particularly high in the accessory olfactory bulb (AOB), a CNS structure critical for detecting chemicals that identify kin and conspecifics. Because of its relative simplicity and its direct projection to the hypothalamus, the AOB provides a model system for studying how mGluRs affect the flow of encoded sensory information to downstream areas. We investigated the role of group I mGluRs in synaptic processing in AOB slices and found that under control conditions, recurrent inhibition of principal neurons (mitral cells) was completely eliminated by the mGluR1 antagonist LY367385 [(S)-(ϩ)-␣-amino-4-carboxy-2 methylbenzeneacetic acid]. In addition, the group I mGluR agonist DHPG [(S)-3,5-dihydroxyphenylglycine; 20 M] induced a dramatic increase in the rate of spontaneous IPSCs. This increase was dependent on voltage-gated calcium channels but persisted even after blockade of ionotropic glutamatergic transmission and sodium channels. Together, these results indicate that mGluR1 plays a critical role in controlling information flow through the AOB and suggest that mGluR1 may be an important locus for experience-dependent changes in synaptic function.

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Section: Mechanisms Of Mglur1 Action In Granule Cellssupporting

confidence: 82%

Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors

Castro¹,

Hovis²,

Urban³

2007

J. Neurosci.

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“…Several studies have reported dendritically localized spiking in GCs, though often involving primarily low-threshold Ca 2+ spikes (Egger et al 2003(Egger et al , 2005. Spontaneous fast Na + -based dendritic spikes have been reported in frog GCs under basal (unstimulated) conditions (Zelles et al 2006). If also present in mammals, spontaneous "D-spikes" could function to synchronize multiple dendrodendritic release sites in one GC, enabling coincident inhibition of nearby pairs of principal cells.…”

Section: Discussionmentioning

confidence: 99%

Modulation of olfactory bulb network activity by serotonin: synchronous inhibition of mitral cells mediated by spatially localized GABAergic microcircuits

Schmidt

Strowbridge

2014

Learn. Mem.

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Although inhibition has often been proposed as a central mechanism for coordinating activity in the olfactory system, relatively little is known about how activation of different inhibitory local circuit pathways can generate coincident inhibition of principal cells. We used serotonin (5-HT) as a pharmacological tool to induce spiking in ensembles of mitral cells (MCs), a primary output neuron in the olfactory bulb, and recorded intracellularly from pairs of MCs to directly assay coincident inhibitory input. We find that 5-HT disynaptically depolarized granule cells (GCs) only slightly but robustly increased the frequency of inhibitory postsynaptic inhibitory currents in MCs. Serotonin also triggered more coincident IPSCs in pairs of nearby MCs than expected by chance, including in MCs with truncated apical dendrites that lack glomerular synapses. That serotonin-triggered coincident inhibition in the absence of elevated GC somatic firing rates suggested that synchronized MC inhibition arose from glutamate receptor-mediated depolarization of GC dendrites or other (non-GC) interneurons outside the glomerular layer. Tetanic stimulation of GCL afferents to GCs triggered robust GC spiking, coincident inhibition in pairs of MCs, and recruited large-amplitude IPSCs in MCs. Enhancing neurotransmission through NMDARs by lowering the external Mg 2+ concentration also increased inhibitory tone onto MCs but failed to promote synchronized inhibition. These results demonstrate that coincident MC inhibition can occur through multiple circuit pathways and suggests that the functional coordination between different GABAergic synapses in individual GCs can be dynamically regulated.Rhythmic sensory input to the olfactory bulb (OB), the secondorder brain region in the olfactory system, recruits complex inhibitory responses (Hamilton and Kauer 1989) that help shape spike patterns of mitral and tufted neurons during basal respiration and sniffing (Abraham et al. 2010). Divergent inhibitory input from granule cells (GCs), the most numerous interneuron subtype within the OB, onto principal cells has been proposed to mediate spike synchronization among subpopulations of principal cells (Galán et al. 2006). However, the ability of GCs, and other bulbar interneurons, to generate coincident inhibition on groups of principal neurons has been studied directly (using paired intracellular recordings) only infrequently.Coincident inhibitory responses onto mitral cells (MCs)-synaptic input that could potentially synchronize firing patterns in output neurons by either resetting intrinsic membrane potential oscillations (Desmaisons et al. 1999) Complicating the interpretation of responses to tetanic stimulation in a resonant brain region such as the OB (Rall and Shepherd 1968;Freeman 1975;Desmaisons et al. 1999;Galán et al. 2006) is the possibility that coincident spiking or synaptic activity following the stimulus might reflect the triggering stimulus rather than synchronization emerging de novo through the intrinsic properties of OB neurons or ...

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“…The fact that latencies are glomerulus specific indicates that the biophysical mechanisms that give rise to the long latencies must be in some respect input specific. This may be attributable to different inputs activating different dendritic branches of the granule cell (Zelles et al, 2006) or otherwise to different properties of synapses onto the granule cells. The biophysical mechanisms underlying this unique behavior are unclear, but understanding them will be important as we try to understand the functional role of granule cells in olfactory bulb circuitry.…”

Section: Discussionmentioning

confidence: 99%

Glomerulus-Specific, Long-Latency Activity in the Olfactory Bulb Granule Cell Network

Kapoor

Urban

2006

J. Neurosci.

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Reliable, stimulus-specific temporal patterns of action potentials have been proposed to encode information in many brain areas, perhaps most notably in the olfactory system. Analysis of such temporal coding has focused almost exclusively on excitatory neurons. Thus, the role of networks of inhibitory interneurons in establishing and maintaining this reliability is unclear. Here we use imaging of population activity in vitro to investigate the mechanisms of temporal pattern generation in mouse olfactory bulb inhibitory interneurons. We show that activity of these interneurons evolves slowly in time but that individual neurons fire at reliable times, with a timescale similar to the slow changes in the patterns of odor-evoked activity and to odor discrimination. Most strikingly, the latency of a single granule cell is highly reliable from trial to trial during repeated stimulation of the same glomerulus, whereas this same cell will have a markedly different latency when a different glomerulus is activated. These data suggest that the timing of granule cell-mediated inhibition in the olfactory bulb is tightly regulated by the source of input and that inhibition may contribute to the generation of reliable temporal patterns of mitral cell activity.

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Branch-Specific Ca²⁺Influx from Na⁺-Dependent Dendritic Spikes in Olfactory Granule Cells

Abstract: Two-photon laser scanning microscopy was used to correlate electrical events detected with whole-cell somatic recordings to Ca

Cited by 56 publications

References 36 publications

Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors

Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors

Modulation of olfactory bulb network activity by serotonin: synchronous inhibition of mitral cells mediated by spatially localized GABAergic microcircuits

Glomerulus-Specific, Long-Latency Activity in the Olfactory Bulb Granule Cell Network

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Branch-Specific Ca2+Influx from Na+-Dependent Dendritic Spikes in Olfactory Granule Cells

Abstract: Two-photon laser scanning microscopy was used to correlate electrical events detected with whole-cell somatic recordings to Ca

Cited by 56 publications

References 36 publications

Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors

Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors

Modulation of olfactory bulb network activity by serotonin: synchronous inhibition of mitral cells mediated by spatially localized GABAergic microcircuits

Glomerulus-Specific, Long-Latency Activity in the Olfactory Bulb Granule Cell Network

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Branch-Specific Ca²⁺Influx from Na⁺-Dependent Dendritic Spikes in Olfactory Granule Cells