Olfactory Bulb Short Axon Cell Release of GABA and Dopamine Produces a Temporally Biphasic Inhibition–Excitation Response in External Tufted Cells

Liu, Shaolin; Plachez, Céline; Shao, Zuoyi; Puché, Adam C.; Shipley, Michael T.

doi:10.1523/jneurosci.3607-12.2013

Cited by 108 publications

(170 citation statements)

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“…It could be the result of a pronounced spikeinduced after-hyperpolarization (AHP) that would be present only when spikes are elicited in MTCs (Dumenieu et al, 2015;Liu et al, 2015). If this were the case, eliminating the IGC-evoked MTC spiking should abolish the following inhibition, as there would be no spike-evoked AHP.…”

Section: Direct Igc Input Produces Long-lasting Inhibition Of Mtcsmentioning

confidence: 99%

“…GABA and DA are coreleased at SAC¡ETC synapses (Borisovska et al, 2013;Liu et al, 2013). DA acts on D1-or D2-like receptors to produce excitatory or inhibitory actions in many other neurons (Beckstead et al, 2004;Govindaiah and Cox, 2005;Liu et al, 2013).…”

Section: Direct Igc Input Produces Long-lasting Inhibition Of Mtcsmentioning

confidence: 99%

“…In the mouse olfactory bulb "short axon cells" (SACs) form the interglomerular circuit (IGC) that interlinks neighboring and distant glomeruli (Aungst et al, 2003;Kosaka and Kosaka, 2008;Kiyokage et al, 2010). IGC acts on glomerular targets by corelease of the inhibitory transmitter, GABA, and the modulatory transmitter, dopamine (DA) (Borisovska et al, 2013; Liu et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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The Interglomerular Circuit Potently Inhibits Olfactory Bulb Output Neurons by Both Direct and Indirect Pathways

2016

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Sensory processing shapes our perception. In mammals, odor information is encoded by combinatorial activity patterns of olfactory bulb (OB) glomeruli. Glomeruli are richly interconnected by short axon cells (SACs), which form the interglomerular circuit (IGC). It is unclear how the IGC impacts OB output to downstream neural circuits. We combined in vitro and in vivo electrophysiology with optogenetics in mice and found the following: (1) the IGC potently and monosynaptically inhibits the OB output neurons mitral/tufted cells (MTCs) by GABA release from SACs: (2) gap junction-mediated electrical coupling is strong for the SAC¡MTC synapse, but negligible for the SAC¡ETC synapse; (3) brief IGC-mediated inhibition is temporally prolonged by the intrinsic properties of MTCs; and (4) sniff frequency IGC activation in vivo generates persistent MTC inhibition. These findings suggest that the temporal sequence of glomerular activation by sensory input determines which stimulus features are transmitted to downstream olfactory networks and those filtered by lateral inhibition.

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Section: Direct Igc Input Produces Long-lasting Inhibition Of Mtcsmentioning

confidence: 99%

Section: Direct Igc Input Produces Long-lasting Inhibition Of Mtcsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Interglomerular Circuit Potently Inhibits Olfactory Bulb Output Neurons by Both Direct and Indirect Pathways

2016

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“…Thus the data suggest that intranasal rotenone administration did not affect the excitability of the MT cells even when rotenone was administered for a longer period. Because DA neurons in the glomerular layer of the OB are thought to be inhibitory interneurons for the MT cells, 17,18) we next recorded the sIPSCs of the MT cells under pharmacological suppression of the excitatory postsynaptic current. The sIPSCs recorded from the MT cells of the rotenone-administered mice showed lower frequency and larger amplitudes than those of the control mice (Fig.…”

Section: Rotenone Administration Altered the Inhibitory Input Into MImentioning

confidence: 99%

Intranasal Administration of Rotenone to Mice Induces Dopaminergic Neurite Degeneration of Dopaminergic Neurons in the Substantia Nigra

Sasajima

Miyazono

Noguchi

et al. 2017

Biological & Pharmaceutical Bulletin

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Exposure to environmental neurotoxins is suspected to be a risk factor for sporadic progressive neurodegenerative diseases. Parkinson's disease has been associated with exposure to the pesticide rotenone, a mitochondrial respiration inhibitor. We previously reported that intranasal administration of rotenone in mice induced dopaminergic (DA) neurodegeneration in the olfactory bulb (OB) and reduced olfactory functions. In the present study, we investigated the DA neurons in the brains of mice that were administered rotenone intranasally for an extended period. We found that the olfactory function of mice was attenuated by rotenone administration. Electrophysiological analysis of the mitral cells, which are output neurons in the OB, revealed that the inhibitory input into the mitral cells was retarded. In the immunohistochemical analysis, neurite degeneration of DA neurons in the substantia nigra was observed in rotenone-administered mice, indicating that rotenone progressively initiated the degeneration of cerebral DA neurons via the nasal route.Key words dopaminergic neuron; intranasal administration; olfactory bulb; rotenone; substantia nigra Environmental chemicals are suspected to be risk factors for neurodegenerative diseases.1) One case control study indicated an association between Parkinson's disease (PD) and the use of a group of pesticides that inhibit mitochondrial complex I, which included rotenone and paraquat.2) PD is characterized by degeneration of dopaminergic (DA) neurons in the substantia nigra pars compacta (SNpc).3) DA neurons are vulnerable to reactive oxygen species (ROS) generated by aberrant mitochondrial respiration.4) Subcutaneous chronic infusion or direct brain infusion of rotenone induces DA neurodegeneration in the substantia nigra (SN) and features of PD in rats, suggesting that exposure to neurotoxins such as rotenone is a risk factor for PD. 5,6) In general, exposure of the human brain to environmental chemicals occurs following the intake of such chemicals by ingestion, cutaneous contact, or inhalation. Various chemicals absorbed at the olfactory mucosa reach the brain directly through passive diffusion from the extra-neural space of olfactory nerves to the cerebrospinal fluid and/or by the active axonal transport of olfactory neurons. 7,8) Prediger et al. postulated that some forms of PD may be caused by environmental agents delivered to the brain via the olfactory mucosa. 9)PD patients often suffer dysosmia as their first symptom. 10)In the olfactory bulb (OB), a primary center for olfactory information processing, DA neurons function as inhibitory interneurons increasing the dynamic range of information transfer from olfactory receptor neurons to OB neurons 11) and maintaining the odor discriminating ability.12) Huisman et al. reported that DA neurons in the OB increased in postmortem autopsy of PD patients, suggesting an increase in inhibitory inputs of dopamine into olfactory nerve terminals could reduce olfactory functions.13) We used one-week rotenone administration to th...

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“…Lateral inhibition is modulated by a variety of inhibitory interneuron subtypes that include superficial short axon cells (Liu et al, 2013;Whitesell et al, 2013;Banerjee et al, 2015), external plexiform layer interneurons (EPL-INs) (Kato et al, 2013;Miyamichi et al, 2013), and granule cells (GCs) (Arevian et al, 2008;Fukunaga et al, 2014;Gschwend et al, 2015). These circuits influence MC/TC activity in a variety of ways that include controlling gain (Banerjee et al, 2015), decorrelating odor representations (Arevian et al, 2008;Giridhar et al, 2011;Gschwend et al, 2015), modulating spike timing (Fukunaga et al, 2014), and synchronizing gamma-frequency oscillations Galán et al, 2006;Lagier et al, 2007;Fukunaga et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Postnatal Odor Exposure Increases the Strength of Interglomerular Lateral Inhibition onto Olfactory Bulb Tufted Cells

Geramita

Urban

2016

J. Neurosci.

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Lateral inhibition between pairs of olfactory bulb (OB) mitral cells (MCs) and tufted cells (TCs) is linked to a variety of computations including gain control, decorrelation, and gamma-frequency synchronization. Differential effects of lateral inhibition onto MCs and TCs via distinct lateral inhibitory circuits are one of several recently described circuit-level differences between MCs and TCs that allow each to encode separate olfactory features in parallel. Here, using acute OB slices from mice, we tested whether lateral inhibition is affected by prior odor exposure and if these effects differ between MCs and TCs. We found that early postnatal odor exposure to the M72 glomerulus ligand acetophenone increased the strength of interglomerular lateral inhibition onto TCs, but not MCs, when the M72 glomerulus was stimulated. These increases were specific to exposure to M72 ligands because exposure to hexanal did not increase the strength of M72-mediated lateral inhibition. Therefore, early life experiences may be an important factor shaping TC odor responses.

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Olfactory Bulb Short Axon Cell Release of GABA and Dopamine Produces a Temporally Biphasic Inhibition–Excitation Response in External Tufted Cells

Cited by 108 publications

References 65 publications

The Interglomerular Circuit Potently Inhibits Olfactory Bulb Output Neurons by Both Direct and Indirect Pathways

The Interglomerular Circuit Potently Inhibits Olfactory Bulb Output Neurons by Both Direct and Indirect Pathways

Intranasal Administration of Rotenone to Mice Induces Dopaminergic Neurite Degeneration of Dopaminergic Neurons in the Substantia Nigra

Postnatal Odor Exposure Increases the Strength of Interglomerular Lateral Inhibition onto Olfactory Bulb Tufted Cells

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