Olfactory Bulb Deep Short-Axon Cells Mediate Widespread Inhibition of Tufted Cell Apical Dendrites

Burton, Shawn D.; LaRocca, Greg; Liu, Annie; Cheetham, Claire E. J.; Urban, Nathaniel N.

doi:10.1523/jneurosci.2880-16.2016

Cited by 45 publications

(56 citation statements)

References 59 publications

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“…The results of our survey of JGCs revealed the presence of two JGC subpopulations with macroscopically similar in their intrinsic physiological features to PG subsets in the MOB (Puopolo and Belluzzi, 1998;Murphy et al, 2005;Sethupathy et al, 2013;Najac et al, 2015;Burton et al, 2017) (Figs. 6-7).…”

Section: Aob Jgcs Include Physiologically-distinct Subsets Associatedmentioning

confidence: 79%

“…The MOB has several interneuron types, collectively termed JGCs, which reside in and around the glomerular layer (Larriva-Sahd, 2008;Yokosuka, 2012). In the MOB, JGCs include excitatory external tufted cells, several types of inhibitory periglomerular cells, and short axon cells (Shipley and Ennis, 1996;Schoppa et al, 1998;Aungst et al, 2003;Parrish-Aungst et al, 2007;Shao et al, 2009;Liu et al, 2013;Najac et al, 2015;Burton et al, 2017;Geramita and Urban, 2017). In the AOB, very few electrophysiological inquiries have been undertaken on JGCs (Goldmakher and Moss, 2000;Hu et al, 2016).…”

Section: Electrophysiological Characteristics Of Aob Jgcsmentioning

confidence: 99%

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Interneuron functional diversity in the mouse accessory olfactory bulb

Maksimova

Cansler

Zuk

et al. 2019

Preprint

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In the mouse accessory olfactory bulb (AOB), inhibitory interneurons play an essential role in gating behaviors elicited by sensory exposure to social odors. Several morphological classes have been described, but the full complement of interneurons remains incomplete. In order to develop a more comprehensive view of interneuron function in the AOB, we performed targeted patch clamp recordings from partially-overlapping subsets of genetically-labeled and morphologically-defined interneuron types. Gad2 (GAD65), Calb2 (calretinin), and Cort (cortistatin)-cre mouse lines were used to drive selective expression of tdTomato in AOB interneurons. Gad2 and Calb2-labeled interneurons were found in the internal, external, and glomerular layers, whereas Cort-labeled interneurons were enriched within the lateral olfactory tract (LOT) and external cellular layer (ECL). We found that external granule cells (EGCs) from all genetically-labeled subpopulations possessed intrinsic functional differences that allowed them to be readily distinguished from internal granule cells (IGCs). EGCs showed stronger voltage-gated Na + and non-inactivating voltage-gated K + currents, decreased I H currents, and robust excitatory synaptic input. These specific intrinsic properties did not correspond to any geneticallylabeled type, suggesting that transcriptional heterogeneity among EGCs and IGCs is not correlated with expression of these particular marker genes. Intrinsic heterogeneity was also seen among AOB juxtaglomerular cells (JGCs), with a major subset of Calb2-labeled JGCs exhibiting spontaneous and depolarization-evoked plateau potentials. These data identify specific physiological features of AOB interneurons types that will assist in future studies of AOB function. Significance Statement:The mouse accessory olfactory bulb (AOB) plays a critical role in processing social chemosensory information. Several morphologically-identified types of AOB inhibitory interneurons are thought to refine and restrict information flow from the AOB to its downstream targets in the limbic system. However, little is known about the electrophysiological and transcriptional diversity among AOB interneuron types. We systematically investigated intrinsic electrophysiological diversity across 5 AOB cell populations in three transgenic mouse lines. Analysis of 26 intrinsic physiological features revealed feature combinations associated with identified morphological AOB cell types, but few associated with the transgenic lines we studied. The results provide quantitative information about functional diversity in AOB interneurons and provide an improved foundation for future studies of AOB circuit function.

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Section: Aob Jgcs Include Physiologically-distinct Subsets Associatedmentioning

confidence: 79%

Section: Electrophysiological Characteristics Of Aob Jgcsmentioning

confidence: 99%

Interneuron functional diversity in the mouse accessory olfactory bulb

Maksimova

Cansler

Zuk

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…; Burton et al . ) and are themselves modulated by basal forebrain inputs. This diversity of olfactory bulb interneurons under the control of basal forebrain fibres makes it challenging to predict the global functional implications of this GABAergic innervation on the olfactory bulb output.…”

Section: Discussionmentioning

confidence: 99%

“…; Burton et al . ) whereas superficial SA cells are tyrosine hydroxylase (TH)‐expressing mixed dopaminergic/GABAergic neurons that regulate glutamate release from OSNs and monosynaptically inhibit external tufted cells (Liu et al . ; Whitesell et al .…”

Section: Introductionmentioning

confidence: 99%

Basal forebrain GABAergic innervation of olfactory bulb periglomerular interneurons

Díez

Najac

Jan

2019

The Journal of Physiology

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Key pointsr Basal forebrain long-range projections to the olfactory bulb are important for olfactory sensitivity and odour discrimination.r Using optogenetics, it was confirmed that basal forebrain afferents mediate IPSCs on granule and deep short axon cells. It was also shown that they selectively innervate specific subtypes of periglomerular (PG) cells.r Three different subtypes of type 2 PG cells receive GABAergic IPSCs from the basal forebrain but not from other PG cells.r Type 1 PG cells, in contrast, do not receive inputs from the basal forebrain but do receive inhibition from other PG cells.r These results shed new light on the complexity and specificity of glomerular inhibitory circuits, as well as on their modulation by the basal forebrain.Abstract Olfactory bulb circuits are dominated by multiple inhibitory pathways that finely tune the activity of mitral and tufted cells, the principal neurons, and regulate odour discrimination. Granule cells mediate interglomerular lateral inhibition between mitral and tufted cells' lateral dendrites whereas diverse subtypes of periglomerular (PG) cells mediate intraglomerular lateral inhibition between their apical dendrites. Deep short axon cells form broad intrabulbar inhibitory circuits that regulate both populations of interneurons. Little is known about the extrabulbar GABAergic circuits that control the activity of these various interneurons. We examined this question using patch-clamp recordings and optogenetics in olfactory bulb slices from transgenic mice. We showed that axonal projections emanating from diverse basal forebrain GABAergic neurons densely project in all layers of the olfactory bulb. These long-range GABAergic projections provide a prominent synaptic input on granule and short axon cells in deep layers as well as on selective subtypes of PG cells. Specifically, three different subclasses of type 2 PG cells receivé Alvaro Sanz Díez obtained his PhD in 2017 from the University of Strasbourg under the supervision of Dr Didier De Saint Jan. There, he studied the inhibitory networks of the mouse olfactory bulb and their connections to the basal forebrain. He is currently a postdoc in Rudy Behnia's lab at Columbia University in New York, where he studies the visual neural networks implicated in colour processing of Drosophila melanogaster. He is interested in how neural circuits encode sensory information and how this is translated behaviourally.A. Sanz Diez and others J Physiol 597.9 robust and target-specific basal forebrain inputs but have little local interactions with other PG cells. In contrast, type 1 PG cells are not innervated by basal forebrain fibres but do interact with other PG cells. Thus, attention-regulated basal forebrain inputs regulate inhibition in all layers of the olfactory bulb with a previously overlooked synaptic complexity that further defines interneuron subclasses.

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“…The spontaneous IPSC frequency was only modestly reduced in visualized MCs with apical dendrites truncated before reaching the glomerular layer, compared with intact MCs, suggesting that most of the inhibitory tone detected in somatic recordings from OB principal cells originates from interneurons outside of the glomerular layer, presumably GCs. While several populations of non-GC interneurons exist in the GCL, these appear to target either TCs (GL-dSACs, 53) or GCs (25, 54). A recent study (55) has found that parvalbumin (PV)-positive interneurons located in the EPL form reciprocal synapses with MCs and, therefore, could also contribute to the inhibitory synchrony we observe.…”

Section: Discussionmentioning

confidence: 99%

Spatial structure of synchronized inhibition in the olfactory bulb

Arnson

Strowbridge

2017

Preprint

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1Olfactory sensory input is detected by receptor neurons in the nose which then send infor-2 mation to the olfactory bulb, the first brain region for processing olfactory information. 3 Within the olfactory bulb, many local circuit interneurons, including axonless granule cells, 4 function to facilitate fine odor discrimination. How interneurons interact with principal 5 cells to affect bulbar processing is not known though the mechanism is likely to be differ-6 ent than in sensory cortical regions since the olfactory bulb lacks an obvious topographical 7 organization; neighboring glomerular columns, representing inputs from different receptor 8 neuron subtypes, typically have different odor tuning. Determining the spatial scale over 9 which interneurons such as granule cells can affect principal cells is a critical step towards 10 understanding how the olfactory bulb operates. We addressed this question by assaying in-11 hibitory synchrony using intracellular recordings from pairs of principal cells with different 12 inter-somatic spacing. We find that in acute rat olfactory bulb slices, inhibitory synchrony 13 is evident in the spontaneous synaptic input in mitral cells separated up to 300 µm. At all 14 inter-somatic spacing assayed, inhibitory synchrony was dependent on fast Na + channels, 15 suggesting that action potentials in granule cells function to coordinate GABA release at rel-16 atively distant dendrodendritic synapses formed throughout the the dendritic arbor. Our 17 results suggest that individual granule cells are able to influence relatively large groups of 18 mitral and tufted cells belonging to clusters of at least 15 glomerular modules, providing a 19 potential mechanism to integrate signals reflecting a wide variety of odorants. 20 Introduction 21Inhibitory local circuits play a central role in processing olfactory information. In insects, 22 blockade of inhibitory function in the antennal lobe, the first processing region of olfactory 23 Coincident inhibition in the OB Page 1 of 26 information, selectively impairs the normal ability of the these animals to make fine distinc-24 tions between related similar odors while leaving intact the ability to distinguish between 25 unrelated olfactory stimuli (1). Recent work in the olfactory bulb, the mammalian equiv-26 alent to the antennal lobe, has demonstrated parallel findings when selectively perturbing 27 inhibition onto the principal neurons mitral (MC) and tufted cells (TC) (2). These studies 28 suggest that olfactory information can be processed through at least two distinct streams -a 29 hardwired pathway that does not require extensive local inhibitory interactions but which 30 reveals only relatively coarse distinctions among odors and a more complex circuit involv-31 ing functions mediated by inhibitory interneurons that facilitates fine distinctions. The lat-32 ter pathway may also be a key site of olfactory learning within the bulb as previous work 33 has found both LTP and spike timing dependent plasticity on excitatory synapse...

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Olfactory Bulb Deep Short-Axon Cells Mediate Widespread Inhibition of Tufted Cell Apical Dendrites

Cited by 45 publications

References 59 publications

Interneuron functional diversity in the mouse accessory olfactory bulb

Interneuron functional diversity in the mouse accessory olfactory bulb

Basal forebrain GABAergic innervation of olfactory bulb periglomerular interneurons

Spatial structure of synchronized inhibition in the olfactory bulb

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