Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil

doi:10.1016/0378-5955(92)90005-8

Hearing Research

Volume 58, Issue 1, February 1992, Pages 26-34

https://doi.org/10.1016/0378-5955(92)90005-8 Get rights and content

Abstract

We made small injections of horseradish peroxidase into the medial superior olivary nucleus (MSO) of gerbils in order to examine the sources of input into that nucleus. As previously described, the MSO receives inputs from neurons in the rostral part of both anteroventral cochlear nuclei. In addition, we found evidence for a projection from the ipsilateral lateral nucleus of the trapezoid body (LNTB). Our results are also compatible with previous reports that the medial nucleus of the trapezoid body (MNTB) projects to the MSO. It is likely that these projections into the MSO from the LNTB and MNTB are sources of inhibitory synaptic inputs.

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Citation Excerpt :
While the MNTB is a rather homogenous population of neurons, the LNTB includes a number of different subregions based on location, inputs and neurochemistry (Spirou and Berrebi, 1996). In animal models, neurons in the posteroventral LNTB (pvLNTB) are glycinergic, receive large calyx terminals from GBCs and project to the ipsilateral MSO (Tolbert et al., 1982; Adams, 1983; Grothe and Sanes, 1993; Spirou et al., 1990, 1998; Smith et al., 1991; Cant and Hyson, 1992; Kuwabara and Zook, 1992; Spirou and Berrebi, 1996, 1997; Franken et al., 2016). While we have previously examined neuronal morphology in the human LNTB, designation into subregions or correlations of cell body morphology was not attempted (Kulesza, 2008).
Localization of sound sources in the environment requires neurons that extract interaural timing differences (ITD) in low-frequency hearing animals from fast and precisely timed converging inputs from both ears. In mammals, this is accomplished by neurons in the medial superior olive (MSO). MSO neurons receive converging excitatory input from both the ipsilateral and contralateral cochlear nuclei and glycinergic, inhibitory input by way of interneurons in the medial and lateral nuclei of the trapezoid body (MNTB and LNTB, respectively). Key features of the ITD circuit are MSO neurons with symmetric dendrites that segregate inputs from the ipsilateral and contralateral ears and preferential distribution of glycinergic inputs on MSO cell bodies. This circuit for ITD is well characterized in gerbils, a mammal with a prominent MSO and a low-frequency hearing range similar to humans. However, the organization of this circuit in the human MSO has not been characterized. This is further complicated by limited understanding of the human LNTB. Nonetheless, we hypothesized that the ITD circuit characterized in laboratory animals is similarly arranged in the human MSO. Herein, we utilized neuron reconstructions and immunohistochemistry to investigate the distribution of glutamatergic and glycinergic inputs onto human MSO neurons. Our results indicate that human MSO neurons have simple, symmetric dendrites and that glycinergic inputs outnumber glutamatergic inputs on MSO cell bodies and proximal dendrites. Together these results suggest that the human MSO utilizes similar circuitry to other mammals with excellent low-frequency hearing.
2.28 - The Superior Olivary Complex
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
This chapter summarized the anatomy and physiology of the four major nuclei in the mammalian superior olivary complex - the medial nucleus of the trapezoid body, the medial and the lateral superior olive, and the superior paraolivary nucleus. The goal of the chapter is to link morphology and synaptic and cellular physiology to the function of these nuclei in sound localization and processing of temporal features of complex sounds.
Neuroanatomical characterization of perineuronal net components in the human cochlear nucleus and superior olivary complex
2018, Hearing Research
Citation Excerpt :
The VCN, for instance, receives glutamatergic input from the auditory nerve (Moore, 1987), but is also innervated by GABA-ergic and glycinergic neurons (Moore et al., 1996; Wu and Oertel, 1986). The MSO receives glutamatergic information from spherical bushy cells from the AVCN (Grothe and Sanes, 1993, 1994; Magnusson et al., 2005; Smith et al., 1998) and bilateral glycinergic input from the MNTB (Kuwabara and Zook, 1992; Stotler, 1953; Werthat et al., 2008) and LNTB (Cant and Hyson, 1992; Grothe et al., 2010). Next, we performed double-label fluorescence immunohistochemistry to investigate the spatial relationship of PNs and synapses in the human VCN and SOC with special focus on differences depending on the predominant neurotransmitter.
The human auditory brainstem, especially the cochlear nucleus (CN) and the superior olivary complex (SOC) are characterized by a high density of neurons associated with perineuronal nets (PNs). PNs build a specific form of extracellular matrix surrounding the neuronal somata, proximal dendrites and axon initial segments. They restrict synaptic plasticity and control high-frequency synaptic activity, a prominent characteristic of neurons of the auditory brainstem. The distribution of PNs within the auditory brainstem has been investigated in a number of mammalian species. However, much less is known regarding PNs in the human auditory brainstem. The present study aimed at the immunohistochemical identification of PNs in the cochlear nucleus (CN) and superior olivary complex (SOC) in the human brainstem. We focused on the complex nature and molecular variability of PNs in the CN and SOC by using specific antibodies against the main PN components (aggrecan, brevican, neurocan and hyaluronan and proteoglycan link protein 1). Virtually all subnuclei within the ventral CN and SOC were found to be associated with PNs. Direct comparison between gerbil and human yielded similar fine structure of PNs and confirmed the typical tight interdigitation of PNs with synaptic terminals in both species. Noticeably, an elaborate combination of immunohistochemical labelings clearly supports the still debated existence of the medial nucleus of trapezoid body (MNTB) in the human brain. In conclusion, the present study demonstrates that PNs form a prominent extracellular structure on CN and SOC neurons in the human brain, potentially stabilizing synaptic contacts, which is in agreement with many other mammalian species.
Glycinergic Inhibitory Plasticity in Binaural Neurons Is Cumulative and Gated by Developmental Changes in Action Potential Backpropagation
2018, Neuron
Citation Excerpt :
Due to the unusually high requirement for precision in this computation, there has been intense interest in understanding how synaptic plasticity can optimize the organization and strength of the underlying circuitry (Gerstner et al., 1996). Inhibitory inputs to MSO neurons arise from the medial and lateral nuclei of the trapezoid body (MNTB and LNTB), modifying binaural information before it is transmitted to higher auditory centers (Cant and Hyson, 1992; Lorteije et al., 2009; Mc Laughlin et al., 2008; Recio-Spinoso, 2012; Roberts et al., 2014; Smith et al., 1991; Spirou et al., 1990). Inhibition, like excitation, is time locked to sub-millisecond precision with auditory stimuli and plays a critical role in sharpening the spatial receptive fields of MSO neurons (Brand et al., 2002; Pecka et al., 2008; Roberts et al., 2014).
Utilization of timing-based sound localization cues by neurons in the medial superior olive (MSO) depends critically on glycinergic inhibitory inputs. After hearing onset, the strength and subcellular location of these inhibitory inputs are dramatically altered, but the cellular processes underlying this experience-dependent refinement are unknown. Here we reveal a form of inhibitory long-term potentiation (iLTP) in MSO neurons that is dependent on spiking and synaptic activation but is not affected by their fine-scale relative timing at higher frequencies prevalent in auditory circuits. We find that iLTP reinforces inhibitory inputs coactive with binaural excitation in a cumulative manner, likely well suited for networks featuring persistent high-frequency activity. We also show that a steep drop in action potential size and backpropagation limits induction of iLTP to the first 2 weeks of hearing. These intrinsic changes would deprive more distal inhibitory synapses of reinforcement, conceivably establishing the mature, soma-biased pattern of inhibition.
Characterization of the superior olivary complex of Canis lupus domesticus
2017, Hearing Research
Citation Excerpt :
We suggest that these CR+ terminals correspond with inputs from globular bushy cells in the ipsilateral VCN as seen in cat (Spirou and Berrebi, 1996). We propose that at least some of the CR+ terminals in the MSO arise from the LNTB, as has been demonstrated in other species (Cant and Hyson, 1992; Kuwabara and Zook, 1992). Goldberg and Brown (1968) found that LNTB neurons (their LPO) received a topographic and strictly ipsilateral projection from the VCN.
The superior olivary complex (SOC) is a collection of brainstem auditory nuclei which play essential roles in the localization of sound sources, temporal coding of vocalizations and descending modulation of the cochlea. Notwithstanding, the SOC nuclei vary considerably between species in accordance with the auditory needs of the animal. The canine SOC was subjected to anatomical and physiological examination nearly 50 years ago and was then virtually forgotten. Herein, we aimed to characterize the nuclei of the canine SOC using quantitative morphometrics, estimation of neuronal number, histochemistry for perineuronal nets and immunofluorescence for the calcium binding proteins calbindin and calretinin. We found the principal nuclei to be extremely well developed: the lateral superior olive (LSO) contained over 20,000 neurons and the medial superior olive (MSO) contained over 15,000 neurons. In nearly all non-chiropterian terrestrial mammals, the MSO exists as a thin, vertical column of neurons. The canine MSO was folded into a U-shaped contour and had associated with the ventromedial tip a small, round collection of neurons we termed the tail nucleus of the MSO. Further, we found evidence within the LSO, MSO and medial nucleus of the trapezoid body (MNTB) for significant morphological variations along the mediolateral or rostrocaudal axes. Finally, the majority of MNTB neurons were calbindin-immunopositive and associated with calretinin-immunopositive calyceal terminals. Together, these observations suggest the canine SOC complies with the basic plan of the mammalian SOC but possesses a number of unique anatomical features.
Auditory System
2015, The Rat Nervous System: Fourth Edition
Sequencing of the rat genome has allowed a better understanding of the rat physiology and biology, in turn promising to translate into a better understanding of human biology and disease processes, including neurobiology of hearing in humans. Sensory cells found in the organ of Corti are known as inner and outer hair cells; they have different functions, and these are discussed in this chapter. The cochlear nuclear complex is the first relay center in the ascending auditory pathway, and the site of termination of all auditory nerve fibers. In the cochlear nuclei, the auditory nerve fibers branch widely and are transmitted to a number of different types of second-order neurons that give rise to a number of parallel ascending tracts, each with a specific pattern of projection into the superior olivary complex, nuclei of the lateral lemniscus and inferior colliculus. The ascending auditory tracts converge towards the auditory midbrain, the inferior colliculus, which is an obligatory relay for many inputs in the route to the auditory cortex. Inferior colliculus neurons project to the medial geniculate body in the thalamus. From the inferior colliculus and upwards, the auditory pathway can be divided into a “lemniscal” projection in which tonotopic organization is very sharp and a “non-lemniscal” projection in which it is less sharp. In contrast to the minimum of two relay stations between the periphery and cerebral cortex in the visual and somatosensory cortices, there is a minimum of three relays in the auditory system, with several stages of convergence and divergence, and at least seven levels in the brainstem where axons cross the midline, making the organization of the auditory system highly complex. Parallel to the ascending pathway, there is a stepwise descending projection from the auditory cortex to the organ of Corti that serve to modulate, filter and/or enhance sound processing in a top-down fashion that clearly plays a critical role in maintaining the normal operations of the auditory system as a whole. A fascinating fact of the auditory system is that it has the extraordinary ability to extract the spectral, temporal and binaural properties of the world around us. From the pattern of sounds reaching our ears, it is possible to identify and distinguish a vast selection of objects. Moreover, our auditory system also provides us with the ability to recognize and communicate through speech, and even enjoy music. Auditory disorders are not fatal per se, but there is little doubt that they can have a devastating effect on our quality of life. This chapter highlights the functional organization of the rat auditory brain, and focuses on the rat as a useful animal model for hearing research. These issues, and more, are discussed in this chapter.

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Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil

Abstract

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Contrib. Sens. Physiol.

Neuroscience

Exp. Neurol.

Neuroscience

Heavy metal intensification of DAB-based HRP reaction product

J. Histochem. Cytochem.

Immunostaining of GABA-ergic and glycinergic inputs to the anteroventral cochlear nucleus

Neurosci. Abstr.

The neuronal architecture of the cochlear nucleus of the cat

J. Comp. Neurol.

Projections to the lateral and medial superior olivary nuclei from the spherical and globular bushy cells of the anteroventral cochlear nucleus

Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei

J. Comp. Neurol.

Neuroanatomical distribution of receptors for three potential inhibitory neurotransmitters in the brainstem auditory nuclei of the cat

J. Comp. Neurol.

Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat

J. Comp. Neurol.

Functional organization of the dog superior olivary complex: An anatomical and electrophysiological study

J. Neurophysiol.

Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization

J. Neurophysiol.

The Auditory Brainstem

Medial and lateral superior olives receive projections from the medial and lateral nuclei of the trapezoid body

Neurosci. Abstr.