Descending projections from the inferior colliculus to medial olivocochlear efferents: Mice with normal hearing, early onset hearing loss, and congenital deafness

Suthakar, Kirupa; Ryugo, David K.

doi:10.1016/j.heares.2016.06.014

Cited by 31 publications

(33 citation statements)

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“…The presynaptic neurons mediating sounddriven MOC activation have been inferred from sound responses; in vivo MOC axon recordings demonstrate sharp frequency tuning and "chopper" firing patterns (Fex, 1962a;Robertson, 1984;Robertson and Gummer, 1985;Liberman and Brown, 1986;Brown, 1989), that, with lesion and tracing studies, suggest primary sound-driven inputs from T-stellate cells of the ventral cochlear nucleus (VCN;Brown et al, 2003Brown et al, , 2013de Venecia et al, 2005;Darrow et al, 2012). Anatomical and functional studies indicate additional synapses onto MOC neurons including from the inferior colliculus, auditory cortex, and nonauditory centers (Faye-Lund, 1986;Caicedo and Herbert, 1993;Thompson and Thompson, 1993;Vetter et al, 1993;Robertson, 2000b, 2002;Groff and Liberman, 2003;Horváth et al, 2003;Ota et al, 2004;Gó mez-Nieto et al, 2008;Brown et al, 2013;Suthakar and Ryugo, 2017). Histochemical staining for neuromodulators and morphological assessment of synapses suggest excitatory, inhibitory, and modulatory inputs to MOC neurons (Helfert et al, 1988;Thompson and Thompson, 1995;Woods and Azeredo, 1999;Mulders and Robertson, 2000a;Benson and Brown, 2006;Suthakar and Ryugo, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…Anatomical and functional studies indicate additional synapses onto MOC neurons including from the inferior colliculus, auditory cortex, and nonauditory centers (Faye-Lund, 1986;Caicedo and Herbert, 1993;Thompson and Thompson, 1993;Vetter et al, 1993;Robertson, 2000b, 2002;Groff and Liberman, 2003;Horváth et al, 2003;Ota et al, 2004;Gó mez-Nieto et al, 2008;Brown et al, 2013;Suthakar and Ryugo, 2017). Histochemical staining for neuromodulators and morphological assessment of synapses suggest excitatory, inhibitory, and modulatory inputs to MOC neurons (Helfert et al, 1988;Thompson and Thompson, 1995;Woods and Azeredo, 1999;Mulders and Robertson, 2000a;Benson and Brown, 2006;Suthakar and Ryugo, 2017). Indeed, excitatory and inhibitory synaptic responses were reported in putative MOC neurons identified post hoc by dendrite morphology (Robertson, 1996).…”

Section: Introductionmentioning

confidence: 99%

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Synaptic Inhibition of Medial Olivocochlear Efferent Neurons by Neurons of the Medial Nucleus of the Trapezoid Body

2019

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Medial olivocochlear (MOC) efferent neurons in the brainstem comprise the final stage of descending control of the mammalian peripheral auditory system through axon projections to the cochlea. MOC activity adjusts cochlear gain and frequency tuning, and protects the ear from acoustic trauma. The neuronal pathways that activate and modulate the MOC somata in the brainstem to drive these cochlear effects are poorly understood. Evidence suggests that MOC neurons are primarily excited by sound stimuli in a three-neuron activation loop from the auditory nerve via an intermediate neuron in the cochlear nucleus. Anatomical studies suggest that MOC neurons receive diverse synaptic inputs, but the functional effect of additional synaptic influences on MOC neuron responses is unknown. Here we use patch-clamp electrophysiological recordings from identified MOC neurons in brainstem slices from mice of either sex to demonstrate that in addition to excitatory glutamatergic synapses, MOC neurons receive inhibitory GABAergic and glycinergic synaptic inputs. These synapses are activated by electrical stimulation of axons near the medial nucleus of the trapezoid body (MNTB). Focal glutamate uncaging confirms MNTB neurons as a source of inhibitory synapses onto MOC neurons. MNTB neurons inhibit MOC action potentials, but this effect depresses with repeat activation. This work identifies a new pathway of connectivity between brainstem auditory neurons and indicates that MOC neurons are both excited and inhibited by sound stimuli received at the same ear. The pathway depression suggests that the effect of MNTB inhibition of MOC neurons diminishes over the course of a sustained sound.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Synaptic Inhibition of Medial Olivocochlear Efferent Neurons by Neurons of the Medial Nucleus of the Trapezoid Body

2019

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“…Only mice that showed an AGS that was tonic in nature on each day of testing were included in this analysis. It should be noted that hearing loss is a common feature with the strains of mice used in AGS studies . However, hearing loss was not a concern in this experiment, as only animals that responded to AGS with a tonic seizure were included in this study.…”

Section: Methodsmentioning

confidence: 99%

“…It should be noted that hearing loss is a common feature with the strains of mice used in AGS studies. [17][18][19] However, hearing loss was not a concern in this experiment, as only animals that responded to AGS with a tonic seizure were included in this study. Therefore, they had to hear the sound stimulation.…”

Section: Experiments 2: An Investigation Of Determinismmentioning

confidence: 99%

Audiogenic seizure as a model of sudden death in epilepsy: A comparative study between four inbred mouse strains from early life to adulthood

et al. 2020

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Objective Mouse models of sudden unexpected death in epileptic patients (SUDEP) using audiogenic seizures (AGS) are valuable because death can occur following a sound‐induced seizure in the absence of any pharmacologic or electric component. However, only a few strains of mice are AGS prone, and the vast majority of studies involve DBA/2 or DBA/1 inbred strains. With the goal of characterizing the variation of AGS susceptibility with age, and of offering a larger panel of mice available for AGS studies, we performed a comparative study of the variability in AGS responses. Methods The variation of AGS with age was determined in two classically used inbred strains of mice, DBA/2 and DBA/1, and two additional strains, BALB/c and 129/SvTer. As AGS‐stimulated tonic seizures can be lethal or nonlethal, even in the same inbred strain, in a second experiment, we addressed whether there is an innate capacity to reproduce the same response after a tonic AGS, referred to as “determinism,” in the DBA/2J, DBA/1J, and 129/SvTer mouse strains. Results Results show that the 129/SvTer mouse is a more versatile model of SUDEP due to its wider age range of susceptibility compared to the DBA/2J and DBA/1J mouse strains. In addition, we show that determinism is not consistently evident in DBA/2J and 129/SvTer strains after AGS. Hence, one cannot be certain that a lethal AGS will always be lethal in successive testing after resuscitation and vice versa in these two mouse strains. Significance These studies highlight the phenotypic variability of AGS in different mouse strains, show the value of an additional mouse strain, 129/SvTer, for studies using AGS, and thus provide valuable information for future studies of AGS and SUDEP.

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“…Ipsilateral and contralateral MOC fibers originate in medial divisions of the superior olivary complex of the brainstem and synapse directly on the basal aspects of OHCs (Warr and Guinan, 1979) to modulate mechanical (Cooper and Guinan, 2006; Murugasu and Russell, 1996) and neural sensitivity to sound (Guinan and Gifford, 1988; Winslow and Sachs, 1987). MOC neurons are also innervated by descending fibers from AC and midbrain neurons, providing a potential means of modulating cochlear activity in a task-related or attention-dependent manner (Faye-Lund, 1986; Mulders and Robertson, 2000; Suthakar and Ryugo, 2017).…”

Section: Introductionmentioning

confidence: 99%

Perceptual gating of a brainstem reflex facilitates speech understanding in human listeners

Hernández-Pérez

Mikiel-Hunter

McAlpine

et al. 2020

Preprint

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14Navigating "cocktail party" situations by enhancing foreground sounds over irrelevant background 15 information is typically considered from a cortico-centric perspective. However, subcortical circuits, 16 such as the medial olivocochlear reflex (MOCR) that modulates inner ear activity itself, have ample 17 opportunity to extract salient features from the auditory scene prior to any cortical processing. To 18 understand the contribution of auditory subcortical nuclei and the cochleae, physiological 19 recordings were made along the auditory pathway while listeners differentiated non(sense)-words 20 and words. Both naturally-spoken and intrinsically-noisy, vocoded speechfiltering that mimics 21 processing by a cochlear implant-significantly activated the MOCR, whereas listening to speech-22 in-background noise revealed instead engagement of midbrain and cortical resources. An auditory 23 periphery model reproduced these speech degradation-specific effects, providing a rationale for 24 goal-directed MOCR gating to enhance representation of speech features in the auditory nerve. 25These results highlight two strategies co-existing in the auditory system to accommodate 26 categorically different speech degradations. 27 78 cortical auditory responses in both the active listening task and when listeners were required to 79 ignore the task and watch a silent, non-subtitled film. 80Maintaining a fixed task difficulty across speech manipulations, we found measures of hearing 81 function at the level of the cochlea, brainstem, midbrain and cortex to be modulated differently 82 depending on the degradation type applied to speech sounds, and on whether or not speech was 83 3 actively attended. Specifically, the MOCR, assessed in terms of the magnitude of click-evoked 84 OAEs (CEOAEs), was activated by vocoded speech-an intrinsically degraded speech signal-but 85 not by otherwise 'clean' speech presented in either babble-noise or speech-shaped noise. Neural 86 activity at the first synaptic stage of central processing in the cochlear nucleus (CN)-assessed 87 physiologically through auditory brainstem responses (ABRs)-confirmed the reduction in cochlear 88 gain for actively attended vocoded speech, but not speech-in-noise. Conversely, neural activity 89 generated by the auditory midbrain was significantly increased in active vs. passive listening for 90 speech in babble and speech-shaped noise, but not for vocoded speech. This increase was 91 associated with elevated cortical markers of listening effort for the speech-in-noise conditions. A 92 model of the auditory periphery including an MOC circuit with biophysically-realistic temporal 93 dynamics confirmed the stimulus-dependent role of the MOCR in enhancing neural coding of 94 speech signals. Our data suggest that otherwise identical performance in active listening tasks may 95 invoke quite different efferent circuits, requiring different levels of listening effort, depending on the 96 type of stimulus degradation experienced. 98 Results 99Iso-performance in three manipul...

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Descending projections from the inferior colliculus to medial olivocochlear efferents: Mice with normal hearing, early onset hearing loss, and congenital deafness

Cited by 31 publications

References 91 publications

Synaptic Inhibition of Medial Olivocochlear Efferent Neurons by Neurons of the Medial Nucleus of the Trapezoid Body

Synaptic Inhibition of Medial Olivocochlear Efferent Neurons by Neurons of the Medial Nucleus of the Trapezoid Body

Audiogenic seizure as a model of sudden death in epilepsy: A comparative study between four inbred mouse strains from early life to adulthood

Perceptual gating of a brainstem reflex facilitates speech understanding in human listeners

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