Histological Determination of the Areas Enriched in Cholinergic Terminals and m2 and m3 Muscarinic Receptors in the Mouse Central Auditory System

Hamada, Satoko; Houtani, Takeshi; Trifonov, Stefan; Kase, Masahiko; Maruyama, Masato; Shimizu, Jun Ichi; Yamashita, Toshio; Tomoda, Koichi; Sugimoto, Tetsuo

doi:10.1002/ar.21186

Cited by 13 publications

(6 citation statements)

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“…In the DCN, combinations of m1–4 mAChR expression have been reported ( Chen et al, 1994 ; Godfrey et al, 1998 ; Irie et al, 2006 ; Pál et al, 2009 ; Zhao and Tzounopoulos, 2011 ; He and Wang, 2014 ). For the AVCN, only the existence of the m2 and m3 subtypes of mAChRs could be shown ( Yao and Godfrey, 1995, 1996 ; Yao et al, 1996 ; Hamada et al, 2010 ). Since the m3 receptor mediates postsynaptic excitation by inhibiting potassium currents ( Brown, 2010 ; Haga, 2013 ), a phenomenon termed the M-current ( Brown and Adams, 1980 ), we hypothesize that the modulation of SBC RMP is caused by m3 mAChR activation.…”

Section: Discussionmentioning

confidence: 99%

“…The remaining cholinergic fibers originate in the pontomesencephalic tegmentum ( Mellott et al, 2011 ) and thus carry only indirectly stimulus-driven information. The presence of both nicotinic acetylcholine (ACh) receptors (nAChRs) and muscarinic ACh receptors (mAChRs) has been shown in VCN on a histological level ( Happe and Morley, 1998 ; Yao and Godfrey, 1999a , b ; Morley and Happe, 2000 ; Morley, 2005 ; Motts et al, 2008 ; Hamada et al, 2010 ; Mellott et al, 2011 ; Schofield et al, 2011 ). Accordingly, acetylcholine can alter the spike rates of neurons in the VCN ( Caspary et al, 1983 ), and the excitatory effects of ACh were shown for T-stellate cells of the VCN ( Fujino and Oertel, 2001 ; Oertel and Fujino, 2001 ; Bal et al, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

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Slow Cholinergic Modulation of Spike Probability in Ultra-Fast Time-Coding Sensory Neurons

Goyer

Kurth

Gillet

et al. 2016

eNeuro

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Sensory processing in the lower auditory pathway is generally considered to be rigid and thus less subject to modulation than central processing. However, in addition to the powerful bottom-up excitation by auditory nerve fibers, the ventral cochlear nucleus also receives efferent cholinergic innervation from both auditory and nonauditory top–down sources. We thus tested the influence of cholinergic modulation on highly precise time-coding neurons in the cochlear nucleus of the Mongolian gerbil. By combining electrophysiological recordings with pharmacological application in vitro and in vivo, we found 55–72% of spherical bushy cells (SBCs) to be depolarized by carbachol on two time scales, ranging from hundreds of milliseconds to minutes. These effects were mediated by nicotinic and muscarinic acetylcholine receptors, respectively. Pharmacological block of muscarinic receptors hyperpolarized the resting membrane potential, suggesting a novel mechanism of setting the resting membrane potential for SBC. The cholinergic depolarization led to an increase of spike probability in SBCs without compromising the temporal precision of the SBC output in vitro. In vivo, iontophoretic application of carbachol resulted in an increase in spontaneous SBC activity. The inclusion of cholinergic modulation in an SBC model predicted an expansion of the dynamic range of sound responses and increased temporal acuity. Our results thus suggest of a top–down modulatory system mediated by acetylcholine which influences temporally precise information processing in the lower auditory pathway.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Slow Cholinergic Modulation of Spike Probability in Ultra-Fast Time-Coding Sensory Neurons

Goyer

Kurth

Gillet

et al. 2016

eNeuro

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“…Since M2 receptors are mainly presynaptic (1, 13) located and inhibitory to neuronal activity, we hypothesized that dialysis of a specific M2 receptor antagonist would reduce inhibition of presynaptic release of excitatory neuromodulators and thus increase breathing. On the other hand, since M3 receptors are predominately postsynaptic (13,27), we performed additional studies to test the hypothesis that dialysis of a specific M3 receptor antagonist should decrease breathing (36). Accordingly, in the same goats used for dialysis of 50 mM atropine, we unilaterally dialyzed a specific M2 antagonist (methoctramine hydrate, 50 mM), or a specific M3 receptor antagonist (4-diphenylacetoxy-N-methylpiperidine methiodide, 5 mM) in the awake state.…”

Section: Effects Of Dialysis Of Antagonists To Receptors For Excitatory Neuromodulators In the Vrcmentioning

confidence: 99%

Julius H. Comroe Distinguished Lecture: Interdependence of neuromodulators in the control of breathing

Forster

2018

Journal of Applied Physiology

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In vitro and in vivo anesthetized studies led to the conclusion that "deficiencies in one neuromodulator are immediately compensated by the action of other neuromodulators" which suggests an interdependence among neuromodulators. This concept was the focus of the 2018 Julius H. Comroe Lecture to the American Physiological Society in which I summarized our published studies testing the hypothesis that if modulatory interdependence was robust, breathing would not decrease during dialysis of antagonists to G protein-coupled excitatory receptors or agonists to inhibitory receptors into the ventral respiratory column (VRC) or the hypoglossal motor nuclei (HMN). We found breathing was not decreased during unilateral VRC dialyses of antagonists to excitatory muscarinic, serotonergic, and neurokinin-1 receptors alone or in combinations, nor was breathing decreased with unilateral VRC dialysis of a µ-opioid receptor agonist. Analyses of the effluent dialysate revealed locally increased serotonin (excitatory) during muscarinic receptor blockade and decreased γ-aminobutyric acid (inhibitory) during dialysis of opioid agonists, suggesting an interdependence of neuromodulators through release of compensatory neuromodulators. Bilateral dialysis of receptor antagonists or agonist in the VRC increased breathing which does not support the concept that unchanged breathing with unilateral dialyses was due to contralateral compensation. In contrast, in the HMN neither unilateral nor bilateral dialysis of the excitatory receptor antagonists altered breathing, but unilateral dialysis of the opioid receptor agonist decreased breathing. We conclude: 1) there is site-dependent interdependence of neuromodulators during physiologic conditions, and 2) attributing physiologic effects to a specific receptor perturbation is complicated by local compensatory mechanisms.

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“…The IClc has also been noted for its comparatively high levels of the α7 nicotinic receptor subunit and high levels of acetylcholinesterase (Happe and Morley, 2004 ; Dillingham et al, 2017 ). Muscarinic receptors also stained differentially in the IC, with an expression of m2 receptors highest in the IClc and ICd and less so in the ICc (Hamada et al, 2010 ). All of this points to a diverse effect of ACh onto several different regions of IC which are known to participate in different parallel ascending auditory and multisensory pathways (Calford and Aitkin, 1983 ; Rouiller, 1997 ; Mellott et al, 2014 ).…”

Section: Introductionmentioning

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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Histological Determination of the Areas Enriched in Cholinergic Terminals and m2 and m3 Muscarinic Receptors in the Mouse Central Auditory System

Cited by 13 publications

References 49 publications

Slow Cholinergic Modulation of Spike Probability in Ultra-Fast Time-Coding Sensory Neurons

Slow Cholinergic Modulation of Spike Probability in Ultra-Fast Time-Coding Sensory Neurons

Julius H. Comroe Distinguished Lecture: Interdependence of neuromodulators in the control of breathing

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

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