A Novel Class of Inferior Colliculus Principal Neurons Labeled in Vasoactive Intestinal Peptide-Cre Mice

Goyer, David; Silveira, Marina A.; George, Alexander P; Beebe, Nichole L.; Edelbrock, Ryan M; Malinski, Peter T; Schofield, Brett R.; Roberts, Michael

doi:10.1101/474312

Cited by 10 publications

(24 citation statements)

References 97 publications

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“…Those experiments were conducted in young animals and could potentially reflect mechanisms that disappear after the system has developed (see Morley and Happe, 2000 for a discussion of separate cholinergic roles during and after the development of the auditory system). In a preliminary study, Rivera-Perez et al ( 2020 ) demonstrated direct nicotinic depolarization of VIP-expressing IC cells (which are known to be glutamatergic; Goyer et al, 2019 ). Additional experiments will be needed to identify the receptor types on glutamatergic and GABAergic IC cells and to differentiate presynaptic vs. postsynaptic effects.…”

Section: Discussionmentioning

confidence: 99%

Cholinergic Projections From the Pedunculopontine Tegmental Nucleus Contact Excitatory and Inhibitory Neurons in the Inferior Colliculus

Noftz

Beebe

Mellott

et al. 2020

Front. Neural Circuits

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The inferior colliculus processes nearly all ascending auditory information. Most collicular cells respond to sound, and for a majority of these cells, the responses can be modulated by acetylcholine (ACh). The cholinergic effects are varied and, for the most part, the underlying mechanisms are unknown. The major source of cholinergic input to the inferior colliculus is the pedunculopontine tegmental nucleus (PPT), part of the pontomesencephalic tegmentum known for projections to the thalamus and roles in arousal and the sleep-wake cycle. Characterization of PPT inputs to the inferior colliculus has been complicated by the mixed neurotransmitter population within the PPT. Using selective viral-tract tracing techniques in a ChAT-Cre Long Evans rat, the present study characterizes the distribution and targets of cholinergic projections from PPT to the inferior colliculus. Following the deposit of viral vector in one PPT, cholinergic axons studded with boutons were present bilaterally in the inferior colliculus, with the greater density of axons and boutons ipsilateral to the injection site. On both sides, cholinergic axons were present throughout the inferior colliculus, distributing boutons to the central nucleus, lateral cortex, and dorsal cortex. In each inferior colliculus (IC) subdivision, the cholinergic PPT axons appear to contact both GABAergic and glutamatergic neurons. These findings suggest cholinergic projections from the PPT have a widespread influence over the IC, likely affecting many aspects of midbrain auditory processing. Moreover, the effects are likely to be mediated by direct cholinergic actions on both excitatory and inhibitory circuits in the inferior colliculus.

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Section: Discussionmentioning

confidence: 99%

Cholinergic Projections From the Pedunculopontine Tegmental Nucleus Contact Excitatory and Inhibitory Neurons in the Inferior Colliculus

Noftz

Beebe

Mellott

et al. 2020

Front. Neural Circuits

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“…This gap in knowledge has eluded the field mostly due to the complexity of the neuronal populations in the IC, where it has proven difficult to identify and study specific neuron classes using conventional approaches. We recently overcame this obstacle, identifying vasoactive intestinal peptide (VIP) neurons as the first molecularly identifiable neuron class in the IC (Goyer et al, 2019). Vasoactive intestinal peptide neurons are found throughout the major IC subdivisions, they are glutamatergic, and they have a stellate morphology with spiny dendrites that, within the central nucleus of the IC (ICc), typically extend across two or more isofrequency laminae.…”

Section: Introductionmentioning

confidence: 99%

α3β4∗ Nicotinic Acetylcholine Receptors Strongly Modulate the Excitability of VIP Neurons in the Mouse Inferior Colliculus

Rivera-Perez

Kwapiszewski

Roberts

2021

Front. Neural Circuits

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The inferior colliculus (IC), the midbrain hub of the central auditory system, receives extensive cholinergic input from the pontomesencephalic tegmentum. Activation of nicotinic acetylcholine receptors (nAChRs) in the IC can alter acoustic processing and enhance auditory task performance. However, how nAChRs affect the excitability of specific classes of IC neurons remains unknown. Recently, we identified vasoactive intestinal peptide (VIP) neurons as a distinct class of glutamatergic principal neurons in the IC. Here, in experiments using male and female mice, we show that cholinergic terminals are routinely located adjacent to the somas and dendrites of VIP neurons. Using whole-cell electrophysiology in brain slices, we found that acetylcholine drives surprisingly strong and long-lasting excitation and inward currents in VIP neurons. This excitation was unaffected by the muscarinic receptor antagonist atropine. Application of nAChR antagonists revealed that acetylcholine excites VIP neurons mainly via activation of α3β4∗ nAChRs, a nAChR subtype that is rare in the brain. Furthermore, we show that acetylcholine excites VIP neurons directly and does not require intermediate activation of presynaptic inputs that might express nAChRs. Lastly, we found that low frequency trains of acetylcholine puffs elicited temporal summation in VIP neurons, suggesting that in vivo-like patterns of cholinergic input can reshape activity for prolonged periods. These results reveal the first cellular mechanisms of nAChR regulation in the IC, identify a functional role for α3β4∗ nAChRs in the auditory system, and suggest that cholinergic input can potently influence auditory processing by increasing excitability in VIP neurons and their postsynaptic targets.

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“…Num. MAB5406, RRID: AB_2278725; Anstotz, Karsak, & Rune, ; Chuhma, Mingote, Moore, & Rayport, ; Goyer et al, ; Orefice et al, ; Tulloch, Teo, Carvajal, Tessier‐Lavigne, & Jaworski, ). GAD67 is an enzyme that catalyzes the synthesis of GABA and encoded by Gad1 gene (Pinal & Tobin, ).…”

Section: Resultsmentioning

confidence: 99%

A cell type‐specific expression map of NCoR1 and SMRT transcriptional co‐repressors in the mouse brain

Iemolo

Montilla‐Perez

Lai

et al. 2020

J of Comparative Neurology

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The ability to rapidly change gene expression patterns is essential for differentiation, development, and functioning of the brain. Throughout development, or in response to environmental stimuli, gene expression patterns are tightly regulated by the dynamic interplay between transcription activators and repressors. Nuclear receptor corepressor 1 (NCoR1) and silencing mediator for retinoid or thyroid-hormone receptors (SMRT) are the best characterized transcriptional co-repressors from a molecular point of view. They mediate epigenetic silencing of gene expression in a wide range of developmental and homeostatic processes in many tissues, including the brain. For instance, NCoR1 and SMRT regulate neuronal stem cell proliferation and differentiation during brain development and they have been implicated in learning and memory. However, we still have a limited understanding of their regional and cell type-specific expression in the brain. In this study, we used fluorescent immunohistochemistry to map their expression patterns throughout the adult mouse brain. Our findings reveal that NCoR1 and SMRT share an overall neuroanatomical distribution, and are detected in both excitatory and inhibitory neurons. However, we observed striking differences in their cell type-specific expression in glial cells. Specifically, all oligodendrocytes express NCoR1, but only a subset express SMRT. In addition, NCoR1, but not SMRT, was detected in a subset of astrocytes and in the microglia. These novel observations are corroborated by single cell transcriptomics and emphasize how NCoR1 and SMRT may contribute to distinct biological functions, suggesting an exclusive role of NCoR1 in innate immune responses in the brain.

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A Novel Class of Inferior Colliculus Principal Neurons Labeled in Vasoactive Intestinal Peptide-Cre Mice

Cited by 10 publications

References 97 publications

Cholinergic Projections From the Pedunculopontine Tegmental Nucleus Contact Excitatory and Inhibitory Neurons in the Inferior Colliculus

Cholinergic Projections From the Pedunculopontine Tegmental Nucleus Contact Excitatory and Inhibitory Neurons in the Inferior Colliculus

α3β4∗ Nicotinic Acetylcholine Receptors Strongly Modulate the Excitability of VIP Neurons in the Mouse Inferior Colliculus

A cell type‐specific expression map of NCoR1 and SMRT transcriptional co‐repressors in the mouse brain

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