scholarly journals Activity-dependent formation and location of voltage-gated sodium channel clusters at a CNS nerve terminal during postnatal development

2017 ◽  
Vol 117 (2) ◽  
pp. 582-593 ◽  
Author(s):  
Jie Xu ◽  
Emmanuelle Berret ◽  
Jun Hee Kim
Keyword(s):  
Brain Stem ◽  
Nerve Terminal ◽  
Low Frequency ◽  
Presynaptic Terminal ◽  
Scaffolding Protein ◽  
Unmyelinated Axon ◽  
Voltage Gated ◽  
Medial Nucleus ◽  
Auditory Brain Stem ◽  
Activity Dependent

In auditory pathways, the precision of action potential (AP) propagation depends on axon myelination and high densities of voltage-gated Na (Nav) channels clustered at nodes of Ranvier. Changes in Nav channel expression at the heminode, the final node before the nerve terminal, can alter AP invasion into the presynaptic terminal. We studied the activity-dependent formation of Nav channel clusters before and after hearing onset at postnatal day 12 in the rat and mouse auditory brain stem. In rats, the Nav channel cluster at the heminode formed progressively during the second postnatal week, around hearing onset, whereas the Nav channel cluster at the nodes was present before hearing onset. Initiation of heminodal Nav channel clustering was correlated with the expression of scaffolding protein ankyrinG and paranodal protein Caspr. However, in whirler mice with congenital deafness, heminodal Nav channels did not form clusters and maintained broad expression, but Nav channel clustering was normal at the nodes. In addition, a clear difference in the distance from the heminodal Nav channel to the calyx across the mediolateral axis of the medial nucleus of the trapezoid body (MNTB) developed after hearing onset. In the medial MNTB, where neurons respond best to high-frequency sounds, the heminodal Nav channel cluster was located closer to the terminal than in the lateral MNTB, where neurons respond best to low-frequency sounds. Thus sound-mediated neuronal activities are potentially associated with the refinement of the heminode adjacent to the presynaptic terminal in the auditory brain stem. NEW & NOTEWORTHY Clustering of voltage-gated sodium (Nav) channels and their distribution along the axon, specifically at the unmyelinated axon segment next to the nerve terminal, are essential for tuning propagated action potentials. Nav channel clusters near the nerve terminal and their location as a function of neuronal position along the mediolateral axis are controlled by auditory inputs after hearing onset. Thus sound-mediated neuronal activity influences the tonotopic organization of Nav channels at the nerve terminal in the auditory brain stem.

Roles of Inhibition in Creating Complex Auditory Responses in the Inferior Colliculus: Facilitated Combination-Sensitive Neurons

2005 ◽  
Vol 93 (6) ◽  
pp. 3294-3312 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Low Frequency ◽  
Auditory Responses ◽  
Auditory Brain Stem ◽  
Neural Interactions ◽  
Lower Brain Stem ◽  
Excitatory Responses ◽  
Sonar Echoes ◽  
Inhibitory Interactions

We studied roles of inhibition on temporally sensitive facilitation in combination-sensitive neurons from the mustached bat's inferior colliculus (IC). In these integrative neurons, excitatory responses to best frequency (BF) tones are enhanced by much lower frequency signals presented in a specific temporal relationship. Most facilitated neurons (76%) showed inhibition at delays earlier than or later than the delays causing facilitation. The timing of inhibition at earlier delays was closely related to the best delay of facilitation, but the inhibition had little influence on the duration or strength of the facilitatory interaction. Local iontophoretic application of antagonists to receptors for glycine (strychnine, STRY) and γ-aminobutyric acid (GABA) (bicuculline, BIC) showed that STRY abolished facilitation in 96% of tested units, but BIC eliminated facilitation in only 28%. This suggests that facilitatory interactions are created in IC and reveals a differential role for these neurotransmitters. The facilitation may be created by coincidence of a postinhibitory rebound excitation activated by the low-frequency signal with the BF-evoked excitation. Unlike facilitation, inhibition at earlier delays was not eliminated by application of antagonists, suggesting an origin in lower brain stem nuclei. However, inhibition at delays later than facilitation, like facilitation itself, appears to originate within IC and to be more dependent on glycinergic than GABAergic mechanisms. Facilitatory and inhibitory interactions displayed by these combination-sensitive neurons encode information within sonar echoes and social vocalizations. The results indicate that these complex response properties arise through a series of neural interactions in the auditory brain stem and midbrain.

Long-Term Depression of Synaptic Inhibition Is Expressed Postsynaptically in the Developing Auditory System

2003 ◽  
Vol 90 (3) ◽  
pp. 1479-1488 ◽  
Author(s):  
Eric H. Chang ◽  
Vibhakar C. Kotak ◽  
Dan H. Sanes
Keyword(s):  
Release Kinetics ◽  
Mean Amplitude ◽  
Ruthenium Red ◽  
Synapse Elimination ◽  
Long Term Depression ◽  
Medial Nucleus ◽  
Auditory Brain Stem ◽  
Pulse Ratio ◽  
Activity Dependent

Inhibitory transmission is critically involved in the functional maturation of neural circuits within the brain. However, the mechanisms involved in its plasticity and development remain poorly understood. At an inhibitory synapse of the developing auditory brain stem, we used whole cell recordings to determine the site of induction and expression of long-term depression (LTD), a robust activity-dependent phenomenon that decreases inhibitory synaptic gain and is postulated to underlie synapse elimination. Recordings were obtained from lateral superior olivary (LSO) neurons, and hyperpolarizing inhibitory potentials were evoked by stimulation of the medial nucleus of the trapezoid body (MNTB). Both postsynaptic glycine and GABAA receptors could independently display LTD when isolated pharmacologically. Focal application of GABA, but not glycine, on the postsynaptic LSO neuron was sufficient to induce depression of the amino acid–evoked response, or MNTB-evoked inhibitory postsynaptic potentials. This GABA-mediated depression, in the absence of MNTB stimulation, was blocked by a GABAB receptor antagonist. To assess whether a change in neurotransmitter release is associated with the LTD, the polyvalent cation, ruthenium red, was used to increase the frequency of miniature inhibitory synaptic events. Consistent with a postsynaptic locus of expression, we found that the mean amplitude of miniature events decreased after LTD with no change in their frequency of occurrence. Furthermore, there was no change in the paired-pulse ratio or release kinetics of evoked inhibitory responses. Together, these results provide direct evidence that activity-dependent LTD of inhibition has a postsynaptic locus of induction and alteration, and that GABA but not glycine plays a pivotal role.

Development of a Robust Central Auditory Synapse in Congenital Deafness

2005 ◽  
Vol 94 (5) ◽  
pp. 3168-3180 ◽  
Author(s):  
M. Youssoufian ◽  
S. Oleskevich ◽  
B. Walmsley
Keyword(s):  
Brain Stem ◽  
Synaptic Strength ◽  
Congenital Deafness ◽  
Calyx Of Held ◽  
Developmentally Regulated ◽  
Release Probability ◽  
Receptor Complexes ◽  
Readily Releasable Pool ◽  
Medial Nucleus ◽  
Auditory Brain Stem

Within the medial nucleus of the trapezoid body (MNTB) in the auditory brain stem, there is a large central synapse known as the calyx of Held, which mediates high-fidelity glutamatergic transmission. We investigated the effects of congenital deafness on the development of pre- and postsynaptic parameters of synaptic strength at the calyx of Held. Whole cell recordings of evoked excitatory postsynaptic currents (EPSCs) and immunohistochemistry of GluR1–4 subunits were performed using brain stem slices from congenitally deaf or hearing mice at postnatal days P5 and P12. In both hearing and deaf mice there was a similar developmental decrease in the NMDA component of the evoked EPSC. There was a concurrent increase in release probability and number of release sites, contributing to a fivefold increase in evoked AMPA-mediated EPSC amplitude. The increase in release probability is opposite to that found in previous studies at the calyx of Held in the rat. There was also a seven- to eightfold increase in the size of the readily releasable pool of vesicles and a decrease in tetanic depression. The postsynaptic glutamate receptor subunits were similarly developmentally regulated and unaffected by deafness. GluR1 and 4 dominated at both ages. There was a decrease in expression of GluR1–3 from P5 to P12 and a shift from GluR2 to GluR3, indicating that AMPA receptor complexes at P12 are predominantly calcium-permeable. These results demonstrate that early development at this robust synapse proceeds normally with congenital deafness, suggesting that auditory nerve activity does not affect the development of synaptic strength at the calyx of Held.

Anatomy and Physiology of Principal Cells of the Medial Nucleus of the Trapezoid Body (MNTB) of the Cat

1998 ◽  
Vol 79 (6) ◽  
pp. 3127-3142 ◽  
Author(s):  
Philip H. Smith ◽  
Philip X. Joris ◽  
Tom C. T. Yin
Keyword(s):  
Brain Stem ◽  
Cell Body ◽  
Superior Olive ◽  
Principal Cells ◽  
Anatomy And Physiology ◽  
Medial Nucleus ◽  
Bushy Cell ◽  
Auditory Brain Stem ◽  
Trapezoid Body ◽  
Bushy Cells

Smith, Philip H., Philip X. Joris, and Tom C. T. Yin. Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J. Neurophysiol. 79: 3127–3142, 1998. We have recorded from principal cells of the medial nucleus of the trapezoid body (MNTB) in the cat's superior olivary complex using either glass micropipettes filled with Neurobiotin or horseradish peroxidase for intracellular recording and subsequent labeling or extracellular metal microelectrodes relying on prepotentials and electrode location. Labeled principal cells had cell bodies that usually gave rise to one or two primary dendrites, which branched profusely in the vicinity of the cell. At the electron microscopic (EM) level, there was a dense synaptic terminal distribution on the cell body and proximal dendrites. Up to half the measured cell surface could be covered with excitatory terminals, whereas inhibitory terminals consistently covered about one-fifth. The distal dendrites were very sparsely innervated. The thick myelinated axon originated from the cell body and innervated nuclei exclusively in the ipsilateral auditory brain stem. These include the lateral superior olive (LSO), ventral nucleus of the lateral lemniscus, medial superior olive, dorsomedial and ventromedial periolivary nuclei, and the MNTB itself. At the EM level the myelinated collaterals gave rise to terminals that contained nonround vesicles and, in the LSO, were seen terminating on cell bodies and primary dendrites. Responses of MNTB cells were similar to their primary excitatory input, the globular bushy cell (GBC), in a number of ways. The spontaneous spike rate of MNTB cells with low characteristic frequencies (CFs) was low, whereas it tended to be higher for higher CF units. In response to short tones, a low frequency MNTB cell showed enhanced phase-locking abilities, relative to auditory nerve fibers. For cells with CFs >1 kHz, the short tone response often resembled the primary-like with notch response seen in many globular bushy cells, with a well-timed onset component. Exceptions to and variations of this standard response were also noted. When compared with GBCs with comparable CFs, the latency of the MNTB cell response was delayed slightly, as would be expected given the synapse interposed between the two cell types. Our data thus confirm that, in the cat, the MNTB receives and converts synaptic inputs from globular bushy cells into a reasonably accurate reproduction of the bushy cell spike response. This MNTB cell output then becomes an important inhibitory input to a number of ipsilateral auditory brain stem nuclei.

Development of Sound Localization Mechanisms in the Mongolian Gerbil Is Shaped by Early Acoustic Experience

2005 ◽  
Vol 94 (2) ◽  
pp. 1028-1036 ◽  
Author(s):  
Armin H. Seidl ◽  
Benedikt Grothe
Keyword(s):  
Brain Stem ◽  
Sound Localization ◽  
Low Frequency ◽  
Mammalian Brain ◽  
Medial Superior Olive ◽  
Visual Inputs ◽  
Auditory Brain Stem ◽  
Barn Owls ◽  
Neuronal Representation ◽  
Acoustic Experience

Sound localization is one of the most important tasks performed by the auditory system. Differences in the arrival time of sound at the two ears are the main cue to localize low-frequency sound in the azimuth. In the mammalian brain, such interaural time differences (ITDs) are encoded in the auditory brain stem; first by the medial superior olive (MSO) and then transferred to higher centers, such as the dorsal nucleus of the lateral lemniscus (DNLL), a brain stem nucleus that gets a direct input from the MSO. Here we demonstrate for the first time that ITD sensitivity in gerbils undergoes a developmental maturation after hearing onset. We further show that this development can be disrupted by altering the animal's acoustic experience during a critical period. In animals that had been exposed to omnidirectional white noise during a restricted time period right after hearing onset, ITD tuning did not develop normally. Instead, it was similar to that of juvenile animals 3 days after hearing onset, with the ITD functions not adjusted to the physiological range. Animals that had been exposed to omnidirectional noise as adults did not show equivalent abnormal ITD tuning. The development presented here is in contrast to that of the development of neuronal representation of ITDs in the midbrain of barn owls and interaural intensity differences in ferrets, where the representations are adjusted by an interaction of auditory and visual inputs. The development of ITD tuning presented here most likely depends on normal acoustic experience and may be related to the maturation of inhibitory inputs to the ITD detector itself.

scholarly journals Can auditory brain stem response accurately reflect the cochlear function?

2020 ◽  
Vol 124 (6) ◽  
pp. 1667-1675
Author(s):  
Dalian Ding ◽  
Jianhui Zhang ◽  
Wenjuan Li ◽  
Dong Li ◽  
Jintao Yu ◽  
...  
Keyword(s):  
Brain Stem ◽  
Damage Model ◽  
Compound Action Potential ◽  
Cochlear Function ◽  
Auditory Brain Stem Response ◽  
Threshold Difference ◽  
Auditory Brain Stem ◽  
Cochlear Damage ◽  
Brain Stem Response ◽  
Compound Action

Auditory brain stem response (ABR) is more commonly used to evaluate cochlear lesions than cochlear compound action potential (CAP). In a noise-induced cochlear damage model, we found that the reduced CAP and enhanced ABR caused the threshold difference. In a unilateral cochlear destruction model, a shadow curve of the ABR from the contralateral healthy ear masked the hearing loss in the destroyed ear.

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