Hyperpolarization-Activated Currents and Subthreshold Resonance in Granule Cells of the Olfactory Bulb

Hu, Ruilong; Ferguson, Katie; Whiteus, Christina; Meijer, Dimphna H.; Araneda, Ricardo C.

doi:10.1523/eneuro.0197-16.2016

Cited by 19 publications

(36 citation statements)

References 67 publications

(88 reference statements)

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“…IGCs are the predominant neuronal type in the AOB, and have been studied more thoroughly than any other interneuron in this circuit (Jia et al, 1999;Taniguchi and Kaba, 2001;Araneda and Firestein, 2006;Smith et al, 2009;Taniguchi et al, 2012;Zimnik et al, 2013;Smith et al, 2015;Hu et al, 2016). These interneurons are thought to play prominent roles in AOB function, including plasticity (Bruce, 1959;Kaba and Keverne, 1988;Brennan et al, 1990;Okutani et al, 2002;Araneda and Firestein, 2006).…”

Section: Electrophysiological Characteristics Of Aob Igcsmentioning

confidence: 99%

“…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). We performed electrophysiological recordings from JGCs in Gad2-, Calb2, and Cort-tdTomato transgenic mice, using the electrophysiological profiling strategy used for IGCs and EGCs (Fig.…”

Section: Electrophysiological Characteristics Of Aob Jgcsmentioning

confidence: 99%

“…IGCs are the most numerous and are currently the best-studied interneuron subtype in the AOB (Dudley and Moss, 1999;Jia et al, 1999;Araneda and Firestein, 2006;Smith et al, 2009;Taniguchi et al, 2012;Hu et al, 2016). Their known and hypothesized connections to experience-dependent plasticity make them a particularly compelling cell type to study (Brennan et al, 1990;Okutani et al, 1999;Cansler et al, 2017;Gao et al, 2017;Oboti et al, 2017).…”

Section: Igc Physiological Diversity Suggests Multiple Functionally-dmentioning

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: Electrophysiological Characteristics Of Aob Igcsmentioning

confidence: 99%

Section: Electrophysiological Characteristics Of Aob Jgcsmentioning

confidence: 99%

Section: Igc Physiological Diversity Suggests Multiple Functionally-dmentioning

confidence: 99%

See 1 more Smart Citation

Interneuron functional diversity in the mouse accessory olfactory bulb

Maksimova

Cansler

Zuk

et al. 2019

Preprint

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“…The frequency at which the maximal impedance is observed is called resonance frequency (f R ), and is set by a combination of passive and active intrinsic membrane properties (Hutcheon & Yarom, 2000). In vitro experiments have shown that most resonant neurons in the mammalian brain display f R s between 2 and 10 Hz: isocortex (Gutfreund et al, 1995;Hutcheon et al, 1996a), thalamus (Puil et al, 1994), hippocampus (Hu et al, 2002), entorhinal cortex (Erchova et al, 2004;Giocomo et al, 2007), amygdala (Pape & Driesang, 1998;Vera et al, 2014) and olfactory bulb (Hu et al, 2016). However, it is not clear whether the differences in f R represent variations in the resonant mechanism or are due to different experimental conditions.…”

Section: Introductionmentioning

confidence: 99%

Neuronal resonance in the theta (4-10 Hz) frequency range is modulated by dynamic changes in the input resistance

Vera

Pereira

Reynaert

et al. 2017

Preprint

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Most neurons of the mammalian brain display intrinsic resonance with frequency selectivity (f R ) for inputs within the theta-range (4-10 Hz). Variations in network oscillation along this range depend on the animal behavior; however, whether neurons can dynamically tune their f R has not been addressed. Using slice electrophysiology, dynamic clamping and computer modeling we studied three types of cortical neurons, finding that the input resistance (R in ) inversely sets f R into the theta range, following a power law. We demonstrate that physiological changes in R in modulate f R and response phase, serving as a mechanism that instantaneously tunes oscillatory responses. Moreover, these modulations are translated into spiking regimes, modifying spike frequency and timing. Since synaptic inputs reduce R in , this modulation provides a mean for adjusting the frequency and timing of firing of individual neurons in interplay with the network fluctuations. This might be a widespread property among resonant neurons.peer-reviewed)

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“…6). HCN channel expression has been noted in the AOB, and in IGCs, but their specific role in AOB circuit function has not yet been determined (Hu et al, 2016). I H is active at resting membrane potential and gives rise to rebound depolarization after relief from transient hyperpolarization (Robinson and Siegelbaum, 2003;Biel et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Experience-dependent plasticity in accessory olfactory bulb interneurons following male-male social interaction

Cansler

Maksimova

Meeks

2017

Preprint

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Chemosensory information processing in the mouse accessory olfactory system (AOS) guides the expression of social behavior. After salient chemosensory encounters, the accessory olfactory bulb (AOB) experiences changes in the balance of excitation and inhibition at reciprocal synapses between mitral cells (MCs) and local interneurons. The mechanisms underlying these changes remain controversial. Moreover, it remains unclear whether MC-interneuron plasticity is unique to specific behaviors, such as mating, or whether it is a more general feature of the AOB circuit. Here, we describe . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/127589 doi: bioRxiv preprint first posted online Apr. 17, 2017; 3 Significance Statement: The accessory olfactory bulb (AOB) is a site of experiencedependent plasticity between excitatory mitral cells (MCs) and inhibitory internal granule cells (IGCs), but the physiological mechanisms and behavioral conditions driving this plasticity remain unclear. Here, we report studies of AOB neuronal plasticity following male-male social chemosensory encounters. We show that the plasticity-associated immediate-early gene Arc is selectively expressed in IGCs from resident males following the resident-intruder assay. After behavior, Arc-expressing IGCs are more strongly excited by sensory input stimulation and MC activation is suppressed. Arcexpressing IGCs do not show increased excitatory synaptic drive, but instead show increased intrinsic excitability. These data indicate that MC-IGC plasticity is induced after male-male social chemosensory encounters, resulting in enhanced MC suppression by Arc-expressing IGCs.

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Hyperpolarization-Activated Currents and Subthreshold Resonance in Granule Cells of the Olfactory Bulb

Cited by 19 publications

References 67 publications

Interneuron functional diversity in the mouse accessory olfactory bulb

Interneuron functional diversity in the mouse accessory olfactory bulb

Neuronal resonance in the theta (4-10 Hz) frequency range is modulated by dynamic changes in the input resistance

Experience-dependent plasticity in accessory olfactory bulb interneurons following male-male social interaction

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