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

Liu, Shaolin; Puché, Adam C.; Shipley, Michael T.

doi:10.1523/jneurosci.1763-16.2016

Cited by 53 publications

(73 citation statements)

References 61 publications

(12 reference statements)

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“…In addition, PGCs are molecularly heterogeneous (Kosaka et al, 1998;Parrish-Aungst et al, 2007;Kiyokage et al, 2010). Alternatively, differences in sSAC-mediated Whitesell et al, 2013;Liu et al, 2016) or ETCmediated (Tatti et al, 2014) inhibition may contribute to differences in glomerular-layer-mediated inhibition onto MCs and TCs. Expressing channelrhodopsin in specific cell types (Fukunaga et al, 2014;Banerjee et al, 2015;Liu et al, 2016) will be vital for determining whether and the extent to which each cell type contributes to differences in inhibition between MCs and TCs.…”

Section: Discussionmentioning

confidence: 99%

“…However, the relative influence of glomerular layer circuits versus GCs in shaping odor-evoked activity in MCs and TCs remains unclear (Cleland, 2010;Fukunaga et al, 2014;Gschwend et al, 2015). Multiple GABAergic interneuron subtypes reside in the glomerular layer, including periglomerular cells (PGCs) (Kiyokage et al, 2010;Shao et al, 2012;Najac et al, 2015), superficial short-axon cells (sSACs) Whitesell et al, 2013;Liu et al, 2016) and even subsets of external tufted cells (ETCs) (Tatti et al, 2014). However, whether differences in the strength of these glomerular layer circuits contribute to differences in the latency of MC and TC responses remains unknown.…”

Section: Introductionmentioning

confidence: 99%

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Differences in Glomerular-Layer-Mediated Feedforward Inhibition onto Mitral and Tufted Cells Lead to Distinct Modes of Intensity Coding

Geramita

Urban

2016

J. Neurosci.

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Understanding how each of the many interneuron subtypes affects brain network activity is critical. In the mouse olfactory system, mitral cells (MCs) and tufted cells (TCs) comprise parallel pathways of olfactory bulb output that are thought to play distinct functional roles in odor coding. Here, in acute mouse olfactory bulb slices, we test how the two major classes of olfactory bulb interneurons differentially contribute to differences in MC versus TC response properties. We show that, whereas TCs respond to olfactory sensory neuron (OSN) stimulation with short latencies regardless of stimulation intensity, MC latencies correlate negatively with stimulation intensity. These differences between MCs and TCs are caused in part by weaker excitatory and stronger inhibitory currents onto MCs than onto TCs. These differences in inhibition between MCs and TCs are most pronounced during the first 150 ms after stimulation and are mediated by glomerular layer circuits. Therefore, blocking inhibition originating in the glomerular layer, but not granule-cell-mediated inhibition, reduces MC spike latency at weak stimulation intensities and distinct temporal patterns of odor-evoked responses in MCs and TCs emerge in part due to differences in glomerular-layer-mediated inhibition.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Differences in Glomerular-Layer-Mediated Feedforward Inhibition onto Mitral and Tufted Cells Lead to Distinct Modes of Intensity Coding

Geramita

Urban

2016

J. Neurosci.

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“…That is not to say that the interglomerular lateral inhibitory synapse may not also be important for phase gating in vivo , but in our simulations here it did not appear to play a prominent role in sensory input gating. Further investigation of how respiration may direct interglomerular inhibition and specifically the role short axon cells may have in modulating PG and external tufted cell activities [35] may aid in understanding their roles in temporal gating of sensory input during each respiratory cycle.…”

Section: Resultsmentioning

confidence: 99%

“…It contained both inter- and intra-glomerular inhibitory synapses, to allow our findings to be generalized to several subtypes of periglomerular cells and short axon cells [31]. There is much diversity in the different juxtaglomerular interneurons in the glomerular layer circuit [31, 35, 53, 54] and inter- and intra-glomerular inhibition likely play distinct roles in sensory processing. With our simulation, we find that sensory evoked phase shifts in MTC activity are predominantly mediated by intraglomerular inhibition (S5 Fig), whereas the addition of ETCs appear to only moderately modulate the strength of tuning (S6 Fig).…”

Section: Discussionmentioning

confidence: 99%

Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb

et al. 2016

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Respiration plays an essential role in odor processing. Even in the absence of odors, oscillating excitatory and inhibitory activity in the olfactory bulb synchronizes with respiration, commonly resulting in a burst of action potentials in mammalian mitral/tufted cells (MTCs) during the transition from inhalation to exhalation. This excitation is followed by inhibition that quiets MTC activity in both the glomerular and granule cell layers. Odor processing is hypothesized to be modulated by and may even rely on respiration-mediated activity, yet exactly how respiration influences sensory processing by MTCs is still not well understood. By using optogenetics to stimulate discrete sensory inputs in vivo, it was possible to temporally vary the stimulus to occur at unique phases of each respiration. Single unit recordings obtained from the mitral cell layer were used to map spatiotemporal patterns of glomerular evoked responses that were unique to stimulations occurring during periods of inhalation or exhalation. Sensory evoked activity in MTCs was gated to periods outside phasic respiratory mediated firing, causing net shifts in MTC activity across the cycle. In contrast, odor evoked inhibitory responses appear to be permitted throughout the respiratory cycle. Computational models were used to further explore mechanisms of inhibition that can be activated by respiratory activity and influence MTC responses. In silico results indicate that both periglomerular and granule cell inhibition can be activated by respiration to internally gate sensory responses in the olfactory bulb. Both the respiration rate and strength of lateral connectivity influenced inhibitory mechanisms that gate sensory evoked responses.

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“…Another circuit involves a class of inhibitory interneuron -short axon cells (SACs) -that branches extensively in the glomerular layer and regulates excitability of mitral/tufted cells in response to sensory input (Aungst et al, 2003;Whitesell et al 2013;Banerjee et al, 2015;Liu et al, 2016). SACs thus constitute the first stage of lateral inhibition in the olfactory system.…”

Section: Introductionmentioning

confidence: 99%

Effect of interglomerular inhibitory networks on olfactory bulb odor representations

Zavitz

Youngstrom

Borisyuk

et al. 2020

Preprint

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Lateral inhibition is a fundamental feature of circuits that process sensory information. In the mammalian olfactory system, inhibitory interneurons called short axon cells comprise the first network mediating lateral inhibition between glomeruli, the functional units of early olfactory coding and processing. The connectivity of this network and its impact on odor representations is not well understood. To explore this question, we constructed a computational model of the interglomerular inhibitory network using detailed characterizations of short axon cell morphologies taken from mouse olfactory bulb. We then examined how this network transformed glomerular patterns of odorant-evoked sensory input (taken from previously-published datasets) as a function of the selectivity of interglomerular inhibition. We examined three connectivity schemes: selective (each glomerulus connects to few others with heterogeneous strength), nonselective (glomeruli connect to most others with heterogenous strength) or global (glomeruli connect to all others with equal strength). We found that both selective and nonselective interglomerular networks could mediate heterogeneous patterns of inhibition across glomeruli when driven by realistic sensory input patterns, but that global inhibitory networks were unable to produce input-output transformations that matched experimental data and were poor mediators of intensitydependent gain control. We further found that networks whose interglomerular connectivity was tuned by sensory input profile decorrelated odor representations more effectively. These results suggest that, despite their multiglomerular innervation patterns, short axon cells are capable of mediating odorant-specific patterns of inhibition between glomeruli that could, theoretically, be tuned by experience or evolution to optimize discrimination of particular odorants.

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

Cited by 53 publications

References 61 publications

Differences in Glomerular-Layer-Mediated Feedforward Inhibition onto Mitral and Tufted Cells Lead to Distinct Modes of Intensity Coding

Differences in Glomerular-Layer-Mediated Feedforward Inhibition onto Mitral and Tufted Cells Lead to Distinct Modes of Intensity Coding

Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb

Effect of interglomerular inhibitory networks on olfactory bulb odor representations

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