Interdependent Conductances Drive Infraslow Intrinsic Rhythmogenesis in a Subset of Accessory Olfactory Bulb Projection Neurons

Gorin, Monika; Tsitoura, Chryssanthi; Kahan, Anat; Watznauer, Katja; Drose, Daniela R.; Arts, Martijn; Mathar, Rudolf; O’Connor, Simon; Hanganu‐Opatz, Ileana L.; Ben‐Shaul, Yoram; Spehr, Marc

doi:10.1523/jneurosci.2520-15.2016

Cited by 27 publications

(40 citation statements)

References 96 publications

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“…Intriguingly, despite the expression of I h , none of the recorded MCs, in either group exhibited subthreshold resonance. Furthermore, while I h has also been observed in AOB MCs (data not shown; but see Gorin et al, 2016), we did not observe subthreshold resonance in recorded AOB MCs ( n = 5) nor in AOB PGCs ( n = 4).…”

Section: Resultssupporting

confidence: 41%

“…However, it has been suggested that MOB MCs exhibit gamma-frequency subthreshold resonance due to a persistent Na + current (Brea et al, 2009), which was not addressed in our studies. Even in the AOB, I h has been described in MCs, but blocking it had no effect on the intrinsic oscillations of MCs (Gorin et al, 2016). In agreement with these findings, we found no I h -mediated subthreshold resonance in AOB MCs.…”

Section: Discussionmentioning

confidence: 99%

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

Ferguson

Whiteus

et al. 2016

eNeuro

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An important contribution to neural circuit oscillatory dynamics is the ongoing activation and inactivation of hyperpolarization-activated currents (Ih). Network synchrony dynamics play an important role in the initial processing of odor signals by the main olfactory bulb (MOB) and accessory olfactory bulb (AOB). In the mouse olfactory bulb, we show that Ih is present in granule cells (GCs), the most prominent inhibitory neuron in the olfactory bulb, and that Ih underlies subthreshold resonance in GCs. In accord with the properties of Ih, the currents exhibited sensitivity to changes in extracellular K+ concentration and ZD7288 (4-ethylphenylamino-1,2-dimethyl-6-methylaminopyrimidin chloride), a blocker of Ih. ZD7288 also caused GCs to hyperpolarize and increase their input resistance, suggesting that Ih is active at rest in GCs. The inclusion of cAMP in the intracellular solution shifted the activation of Ih to less negative potentials in the MOB, but not in the AOB, suggesting that channels with different subunit composition mediate Ih in these regions. Furthermore, we show that mature GCs exhibit Ih-dependent subthreshold resonance in the theta frequency range (4–12 Hz). Another inhibitory subtype in the MOB, the periglomerular cells, exhibited Ih-dependent subthreshold resonance in the delta range (1–4 Hz), while principal neurons, the mitral cells, do not exhibit Ih-dependent subthreshold resonance. Importantly, Ih size, as well as the strength and frequency of resonance in GCs, exhibited a postnatal developmental progression, suggesting that this development of Ih in GCs may differentially contribute to their integration of sensory input and contribution to oscillatory circuit dynamics.

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Section: Resultssupporting

confidence: 41%

Section: Discussionmentioning

confidence: 99%

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

Ferguson

Whiteus

et al. 2016

eNeuro

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“…We observed less evoked spiking activity in MCs in AOB slices taken from post-behavior resident males than no-intruder controls (repeated measures ANOVA, interaction between group and stimulus, F(59,1298)=2.45, p<0.0001, n=13 cells, 4 mice for "intruder" group; n=9 cells, 4 mice for "no intruder" group, Fig. 7B-C Importantly, these currents are much smaller than those observed in IGCs, consistent with recent observations in mitral cells (Gorin et al, 2016). These results confirm that male-male social chemosensory encounters are associated with subsequent MC suppression, consistent with an experience-dependent increase in IGC-MC inhibition.…”

Section: Responses To Glomerular Stimulation Are Suppressed Followsupporting

confidence: 89%

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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“…6C, D). We first found that resting membrane potentials in EGCs (-86.0 mV ± 1.5 mV, n=13) were significantly hyperpolarized compared to MCs (-61.3± 1.0 mV, n=11), confirming earlier results (Gorin et al, 2016;Maksimova et al, 2019). In current clamp mode, standardized ramps of current injection resulted comparable maximal spike frequencies in EGCs (22-32 Hz, n = 4) and MCs (16-34 Hz, n = 5; Fig.…”

Section: Egc and Mcs Gcamp6f Signals Differentially Report Electrophysupporting

confidence: 85%

Paradoxically sparse chemosensory tuning in broadly-integrating external granule cells in the mouse accessory olfactory bulb

Zhang

Meeks

2019

Preprint

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The accessory olfactory bulb (AOB) is a critical circuit in the mouse accessory olfactory system (AOS), but AOB processing is poorly understood compared to the main olfactory bulb (MOB). We used 2-photon GCaMP6f Ca 2+ imaging in an ex vivo preparation to study the chemosensory tuning of AOB external granule cells (EGCs), an interneuron population hypothesized to broadly integrate from mitral cells (MCs). We measured MC and EGC tuning to natural chemosignal blends and monomolecular ligands, finding that EGC tuning was far sparser than MC tuning. Simultaneous patch-clamp electrophysiology and Ca 2+ imaging indicated that this was only partially explained by lower GCaMP6f-to-spiking ratios in EGCs compared to MCs. Ex vivo patch-clamp recordings revealed that EGC subthreshold responsivity was broad, but monomolecular ligand responses were insufficient to elicit spiking. These results indicate that EGC spiking is selectively engaged by chemosensory blends, suggesting different roles for EGCs than analogous interneurons in the MOB. 2005; Kaba and Huang, 2005; Araneda and Firestein, 2006; Hendrickson et al., 2008; Cansler et al., 2017; Gao et al., 2017). Cumulatively, these observations suggest that MC-interneuron communication in the AOB is critical for rodent physiology and behavior. Despite recent progress, many gaps in our understanding of AOB MC-interneuron interactions remain. A major limitation for our understanding of AOB function is a lack of information about how MCs interact with several inhibitory neural types. The AOB has a variety of interneurons that have been largely classified based on their location and morphology (Larriva-Sahd, 2008; Moriya-Ito et al., 2013). Three major AOB interneuron types have been identified, along with several minor types. Juxtaglomerular cells (JGCs) are found within the superficial glomerular layer, where excitatory sensory inputs from the vomeronasal organ (VNO) enter the AOB. External granule cells (EGC) are found in the external cell layer alongside the somas of MCs. Internal granule cells (IGCs), the most abundant and well-studied AOB interneuron type, are located in the internal granule layer. JGCs, similar to counterparts in the main olfactory bulb (MOB), are thought to modulate the input to the MCs via their synaptic connection with VNO axon terminals and MC apical dendrites within glomeruli (Geramita and Urban, 2017). EGCs and IGCs, in contrast, are thought to modulate MC activity via reciprocal dendrodendritic connections (Taniguchi and Kaba, 2001; Castro et al., 2007). Relative to JGCs and IGCs, there is very little information about the physiology or function of AOB EGCs; just one targeted study of their intrinsic features has been reported (Maksimova et al., 2019).Cells that appear analogous to AOB EGCs have been studied in the MOB. Specifically, MOB parvalbumin-expressing interneurons in the external plexiform layer (PV-EPL interneurons) resemble EGCs in their morphologies and apparent broad connectivity with MCs. These MOB PV-EPL interneurons were shown to integr...

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Interdependent Conductances Drive Infraslow Intrinsic Rhythmogenesis in a Subset of Accessory Olfactory Bulb Projection Neurons

Cited by 27 publications

References 96 publications

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

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

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

Paradoxically sparse chemosensory tuning in broadly-integrating external granule cells in the mouse accessory olfactory bulb

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