Intercollicular commissural connections refine the representation of sound frequency and level in the auditory midbrain

Orton, Llwyd David; Rees, Adrian

doi:10.7554/elife.03764

Cited by 21 publications

(28 citation statements)

References 61 publications

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“…The activation of NMDA receptors in our recordings may indicate that excitatory commissural synapses tend to be located on the distal dendrites or dendritic spines of VIP neurons, where the local membrane potential might be sufficiently depolarized by activation of AMPA receptors to remove Mg 2+ block of NMDA receptors. A distal location would be consistent with the proposed modulatory role for commissural inputs (Orton et al, 2016; Orton and Rees, 2014). Similarly, the lack of NMDA receptor activation by DCN afferents might indicate that DCN synapses are located on proximal dendrites or possibly on the soma itself, or that these synapses lack NMDA receptors.…”

Section: Discussionsupporting

confidence: 76%

A novel class of inferior colliculus principal neurons labeled in vasoactive intestinal peptide-Cre mice

Goyer

Silveira

George

et al. 2019

eLife

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Located in the midbrain, the inferior colliculus (IC) is the hub of the central auditory system. Although the IC plays important roles in speech processing, sound localization, and other auditory computations, the organization of the IC microcircuitry remains largely unknown. Using a multifaceted approach in mice, we have identified vasoactive intestinal peptide (VIP) neurons as a novel class of IC principal neurons. VIP neurons are glutamatergic stellate cells with sustained firing patterns. Their extensive axons project to long-range targets including the auditory thalamus, auditory brainstem, superior colliculus, and periaqueductal gray. Using optogenetic circuit mapping, we found that VIP neurons integrate input from the contralateral IC and the dorsal cochlear nucleus. The dorsal cochlear nucleus also drove feedforward inhibition to VIP neurons, indicating that inhibitory circuits within the IC shape the temporal integration of ascending inputs. Thus, VIP neurons are well-positioned to influence auditory computations in a number of brain regions.

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Section: Discussionsupporting

confidence: 76%

A novel class of inferior colliculus principal neurons labeled in vasoactive intestinal peptide-Cre mice

Goyer

Silveira

George

et al. 2019

eLife

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“…The eFRAs recorded with multi-channel silicone electrodes were relatively homogenous and V shaped. This contrasts with the variety of eFRA shapes for single units recorded with tungsten or glass electrodes we and others have previously reported (LeBeau et al, 2001;Palmer et al, 2013;Orton & Rees, 2014;Vogler et al, 2014). The difference most likely reflects the fact that the relatively low impedance silicone electrodes, used here, pick up multiple units such that an average V shaped eFRA dominates, whereas higher impedance electrodes can pick up spikes from single units which vary in the shape of their eFRA.…”

Section: Resultscontrasting

confidence: 83%

Nitric oxide signalling underlies salicylate-induced increases in neuronal firing in the inferior colliculus: a central mechanism of tinnitus?

Olthof

Lyzwa

Gartside

et al. 2021

Preprint

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The tinnitus-inducing agent salicylate reduces cochlear output but causes hyperactivity in higher auditory centres, including the inferior colliculus (the auditory midbrain). Using multi-electrode recording in anaesthetised guinea pigs (Cavia porcellus), we addressed the hypothesis that salicylate-induced hyperactivity in the inferior colliculus involves nitric oxide signalling secondary to increased ascending excitatory input. In the inferior colliculus, systemic salicylate (200 mg/kg i.p., 0 h) markedly increased spontaneous and sound-driven neuronal firing (3-6 h post drug) with both onset and sustained responses to pure tones being massively increased. Reverse microdialysis of increasing concentrations of salicylate directly into the inferior colliculus (100 μM-10 mM, from 0 h) failed to mimic systemic salicylate. In contrast, it caused a small, transient, increase in sound-driven firing (1 h), followed by a larger sustained decrease in both spontaneous and sound-driven firing (2-5 h). When salicylate was given systemically, reverse microdialysis of the neuronal nitric oxide synthase inhibitor L-methyl arginine into the inferior colliculus (500 mM, 2-6 h) completely blocked the salicylate-induced increase in spontaneous and sound-driven neuronal firing. Our data indicate that systemic salicylate induces neuronal hyperactivity in the auditory midbrain via a mechanism outside the inferior colliculus, presumably upstream in the auditory pathway; and that the mechanism is ultimately dependent on nitric oxide signalling within the inferior colliculus. Given that nitric oxide is known to mediate NMDA receptor signalling in the inferior colliculus, we propose that salicylate activates an ascending glutamatergic input to the inferior colliculus and that this is an important mechanism underlying salicylate-induced tinnitus.

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“…The 410 activation of NMDA receptors in our recordings may indicate that excitatory commissural synapses tend 411 to be located on the distal dendrites or dendritic spines of VIP neurons, where the local membrane 412 potential might be sufficiently depolarized by activation of AMPA receptors to remove Mg 2+ block of 413 NMDA receptors. A distal location would be consistent with the proposed modulatory role for 414 commissural inputs(Orton et al, 2016;Orton and Rees, 2014). Similarly, the lack of NMDA receptor 415 activation by DCN afferents might indicate that DCN synapses are located proximal to the soma, possibly 416 on the soma itself, or that these synapses lack NMDA receptors.…”

mentioning

confidence: 67%

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

Goyer

Silveira

George

et al. 2018

Preprint

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10Located in the midbrain, the inferior colliculus (IC) is the hub of the central auditory system. Although 11 the IC plays important roles in speech processing, sound localization, and other auditory computations, 12 the organization of the IC microcircuitry remains largely unknown. Using a multifaceted approach in 13 mice, we have identified vasoactive intestinal peptide (VIP) neurons as a novel class of IC principal 14 neurons. VIP neurons are glutamatergic stellate cells with sustained firing patterns. Their extensive 15 axons project to long-range targets including the auditory thalamus, auditory brainstem, superior 16 colliculus, and periaqueductal gray. Using optogenetic circuit mapping, we found that VIP neurons 17 integrate input from the contralateral IC and the dorsal cochlear nucleus. The dorsal cochlear nucleus 18 also drove feedforward inhibition to VIP neurons, indicating that inhibitory circuits within the IC shape 19 the temporal integration of ascending inputs. Thus, VIP neurons are well-positioned to influence 20 auditory computations in a number of brain regions. 21 Results 67The VIP-IRES-Cre mouse line labels neurons in multiple subdivisions of the IC 68 By crossing VIP-IRES-Cre mice with Ai14 reporter mice, we obtained mice in which VIP + neurons 69 expressed the fluorescent protein tdTomato. VIP + neurons in these animals were visible in numerous 70 brain regions; the present report focuses on the IC. Figure 1 shows the distribution of VIP + neurons 71 (magenta) in transverse sections through the IC. Labeled neurons were present throughout most of the 72 rostro-caudal extent of the IC, but were most numerous in the caudal regions. Labeled neurons were 73 rare or absent in the IC rostral pole and intercollicular tegmentum. 74 75 VIP neurons are glutamatergic and represent 1.8% of IC neurons 76 Previous studies have shown that IC neurons are either glutamatergic or GABAergic (Merchán et al., 77 2005; Oliver et al. , 1994). To investigate the neurotransmitter content of VIP neurons, we performed 78 immunohistochemical staining against GAD67, a marker for GABAergic neurons, in brain slices from 79 three VIP-IRES-Cre x Ai14 animals, aged P58 (Figure 2A). We then counted tdTomato + neurons and 80 GAD67-labeled cell bodies in one caudal and one rostral IC slice per animal. Neurons located in the ICc, 81ICd, and IClc were combined for this analysis. Across 793 tdTomato + neurons, only 10 neurons co-82 VIP neurons exhibit sustained firing patterns and their intrinsic physiology varies along 101the tonotopic axis of the ICc 102Next, we investigated the firing pattern and intrinsic physiology of VIP neurons by targeting whole cell 103 patch clamp recordings to tdTomato + neurons in brain slices from VIP-IRES-Cre x Ai14 mice. Recordings 104 made from the ICc, ICd, and IClc were lumped together for this experiment because there were no clear 105 differences in VIP neuron physiology across these subdivisions of the IC. VIP neurons had a resting 106 membrane potential of -69.5 mV ± 4.4 mV (n = 216, correc...

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Intercollicular commissural connections refine the representation of sound frequency and level in the auditory midbrain

Cited by 21 publications

References 61 publications

A novel class of inferior colliculus principal neurons labeled in vasoactive intestinal peptide-Cre mice

A novel class of inferior colliculus principal neurons labeled in vasoactive intestinal peptide-Cre mice

Nitric oxide signalling underlies salicylate-induced increases in neuronal firing in the inferior colliculus: a central mechanism of tinnitus?

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

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