Short-term synaptic plasticity in the auditory brain stem by using in-vivo-like stimulation parameters

2011 ◽  
Vol 279 (1-2) ◽  
pp. 51-59 ◽  
Author(s):  
Achim Klug
2007 ◽  
Vol 97 (4) ◽  
pp. 2863-2874 ◽  
Author(s):  
K. M. MacLeod ◽  
T. K. Horiuchi ◽  
C. E. Carr

The nature of the synaptic connection from the auditory nerve onto the cochlear nucleus neurons has a profound impact on how sound information is transmitted. Short-term synaptic plasticity, by dynamically modulating synaptic strength, filters information contained in the firing patterns. In the sound-localization circuits of the brain stem, the synapses of the timing pathway are characterized by strong short-term depression. We investigated the short-term synaptic plasticity of the inputs to the bird's cochlear nucleus angularis (NA), which encodes intensity information, by using chick embryonic brain slices and trains of electrical stimulation. These excitatory inputs expressed a mixture of short-term facilitation and depression, unlike those in the timing nuclei that only depressed. Facilitation and depression at NA synapses were balanced such that postsynaptic response amplitude was often maintained throughout the train at high firing rates (>100 Hz). The steady-state input rate relationship of the balanced synapses linearly conveyed rate information and therefore transmits intensity information encoded as a rate code in the nerve. A quantitative model of synaptic transmission could account for the plasticity by including facilitation of release (with a time constant of ∼40 ms), and a two-step recovery from depression (with one slow time constant of ∼8 s, and one fast time constant of ∼20 ms). A simulation using the model fit to NA synapses and auditory nerve spike trains from recordings in vivo confirmed that these synapses can convey intensity information contained in natural train inputs.


2018 ◽  
Author(s):  
Abed Ghanbari ◽  
Naixin Ren ◽  
Christian Keine ◽  
Carl Stoelzel ◽  
Bernhard Englitz ◽  
...  

AbstractInformation transmission in neural networks is influenced by both short-term synaptic plasticity (STP) as well as non-synaptic factors, such as after-hyperpolarization currents and changes in excitability. Although these effects have been widely characterized in vitro using intracellular recordings, how they interact in vivo is unclear. Here we develop a statistical model of the short-term dynamics of spike transmission that aims to disentangle the contributions of synaptic and non-synaptic effects based only on observed pre- and postsynaptic spiking. The model includes a dynamic functional connection with short-term plasticity as well as effects due to the recent history of postsynaptic spiking and slow changes in postsynaptic excitability. Using paired spike recordings, we find that the model accurately describes the short-term dynamics of in vivo spike transmission at a diverse set of identified and putative excitatory synapses, including a thalamothalamic connection in mouse, a thalamocortical connection in a female rabbit, and an auditory brainstem synapse in a female gerbil. We illustrate the utility of this modeling approach by showing how the spike transmission patterns captured by the model may be sufficient to account for stimulus-dependent differences in spike transmission in the auditory brainstem (endbulb of Held). Finally, we apply this model to large-scale multi-electrode recordings to illustrate how such an approach has the potential to reveal cell-type specific differences in spike transmission in vivo. Although short-term synaptic plasticity parameters estimated from ongoing pre- and postsynaptic spiking are highly uncertain, our results are partially consistent with previous intracellular observations in these synapses.Significance StatementAlthough synaptic dynamics have been extensively studied and modeled using intracellular recordings of post-synaptic currents and potentials, inferring synaptic effects from extracellular spiking is challenging. Whether or not a synaptic current contributes to postsynaptic spiking depends not only on the amplitude of the current, but also on many other factors, including the activity of other, typically unobserved, synapses, the overall excitability of the postsynaptic neuron, and how recently the postsynaptic neuron has spiked. Here we developed a model that, using only observations of pre- and postsynaptic spiking, aims to describe the dynamics of in vivo spike transmission by modeling both short-term synaptic plasticity and non-synaptic effects. This approach may provide a novel description of fast, structured changes in spike transmission.


2007 ◽  
Vol 97 (2) ◽  
pp. 1775-1785 ◽  
Author(s):  
Keith N. Darrow ◽  
Stéphane F. Maison ◽  
M. Charles Liberman

Cochlear sensory cells and neurons receive efferent feedback from the olivocochlear (OC) system. The myelinated medial component of the OC system and its effects on outer hair cells (OHCs) have been implicated in protection from acoustic injury. The unmyelinated lateral (L)OC fibers target ipsilateral cochlear nerve dendrites and pharmacological studies suggest the LOC's dopaminergic component may protect these dendrites from excitotoxic effects of acoustic overexposure. Here, we explore LOC function in vivo by selective stereotaxic destruction of LOC cell bodies in mouse. Lesion success in removing the LOC, and sparing the medial (M)OC, was assessed by histological analysis of brain stem sections and cochlear whole mounts. Auditory brain stem responses (ABRs), a neural-based metric, and distortion product otoacoustic emissions (DPOAEs), an OHC-based metric, were measured in control and surgical mice. In cases where the LOC was at least partially destroyed, there were increases in suprathreshold neural responses that were frequency- and level-independent and not attributable to OHC-based effects. These interaural response asymmetries were not found in controls or in cases where the lesion missed the LOC. In LOC-lesion cases, after exposure to a traumatic stimulus, temporary threshold shifts were greater in the ipsilateral ear, but only when measured in the neural response; OHC-based measurements were always bilaterally symmetric, suggesting OHC vulnerability was unaffected. Interaural asymmetries in threshold shift were not found in either unlesioned controls or in cases that missed the LOC. These findings suggest that the LOC modulates cochlear nerve excitability and protects the cochlea from neural damage in acute acoustic injury.


2006 ◽  
Vol 398 (1-2) ◽  
pp. 73-77 ◽  
Author(s):  
Fan Jia ◽  
Haiyang Wei ◽  
Xiangrui Li ◽  
Xiaoqiao Xie ◽  
Yifeng Zhou

2012 ◽  
Vol 108 (11) ◽  
pp. 2999-3008 ◽  
Author(s):  
Stefan J. Mauger ◽  
Mohit N. Shivdasani ◽  
Graeme D. Rathbone ◽  
Antonio G. Paolini

The auditory brain stem implant (ABI) is being used clinically to restore hearing to patients unable to benefit from a cochlear implant (CI). Speech perception outcomes for ABI users are typically poor compared with most CI users. The ABI is implanted either on the surface of or penetrating through the cochlear nucleus in the auditory brain stem and uses stimulation strategies developed for auditory nerve stimulation with a CI. Although the stimulus rate may affect speech perception outcomes with current stimulation strategies, no studies have systematically investigated the effect of stimulus rate electrophysiologically or clinically. We therefore investigated rate response properties and temporal response properties of single inferior colliculus (IC) neurons from penetrating ABI stimulation using stimulus rates ranging from 100 to 1,600 pulses/s in the rat. We found that the stimulus rate affected the proportion of response types, thresholds, and dynamic ranges of IC activation. The stimulus rate was also found to affect the temporal properties of IC responses, with higher rates providing more temporally similar responses to acoustic stimulation. Suppression of neural firing and inhibition in IC neurons was also found, with response properties varying with the stimulus rate. This study demonstrated that changes in the ABI stimulus rate results in significant differences in IC neuron response properties. Due to electrophysiological differences, the stimulus rate may also change perceptual properties. We suggest that clinical evaluation of the ABI stimulus rate should be performed.


2012 ◽  
Vol 24 (10) ◽  
pp. 2579-2603 ◽  
Author(s):  
Tyler P. Lee ◽  
Dean V. Buonomano

The discrimination of complex auditory stimuli relies on the spatiotemporal structure of spike patterns arriving in the cortex. While recordings from auditory areas reveal that many neurons are highly selective to specific spatiotemporal stimuli, the mechanisms underlying this selectivity are unknown. Using computer simulations, we show that selectivity can emerge in neurons in an entirely unsupervised manner. The model is based on recurrently connected spiking neurons and synapses that exhibit short-term synaptic plasticity. During a developmental stage, spoken digits were presented to the network; the only type of long-term plasticity present was a form of homeostatic synaptic plasticity. From an initially unresponsive state, training generated a high percentage of neurons that responded selectively to individual digits. Furthermore, units within the network exhibited a cardinal feature of vocalization-sensitive neurons in vivo: differential responses between forward and reverse stimulus presentations. Direction selectivity deteriorated significantly, however, if short-term synaptic plasticity was removed. These results establish that a simple form of homeostatic plasticity is capable of guiding recurrent networks into regimes in which complex stimuli can be discriminated. In addition, one computational function of short-term synaptic plasticity may be to provide an inherent temporal asymmetry, thus contributing to the characteristic forward-reverse selectivity.


2002 ◽  
Vol 111 (11) ◽  
pp. 1008-1014 ◽  
Author(s):  
Hung Thai-Van ◽  
Stéphane Gallego ◽  
Evelyne Veuillet ◽  
Eric Truy ◽  
Lionel Collet

Bilateral cochlear implantation provides an interesting model for in vivo study of the effect of long-term profound deafness on neural transmission. We present electrophysiological observations on 2 patients implanted with the MXM Binaural Digisonic Convex system. This uncommon design consists of 2 electrode arrays placed bilaterally into the scala tympani and controlled by a single speech processor. In both patients, the duration of deafness before cochlear implantation clearly differed from one ear to the other. Electrically evoked auditory brain stem responses (EABRs) were measured and the EABRs from the ear with the longer deafness duration showed a lengthening of wave V latency. In 1 patient, recordings from this ear also showed a lack of reproducibility of wave III. The data suggest that neural responsiveness in the peripheral and intermediate auditory pathways is adversely affected by deafness duration. Poor EABRs on one ear possibly result from the total duration of deafness in this ear and/or compensation by the other ear.


2016 ◽  
Vol 115 (4) ◽  
pp. 2033-2051 ◽  
Author(s):  
Joshua H. Goldwyn ◽  
John Rinzel

The ongoing activity of neurons generates a spatially and time-varying field of extracellular voltage ( Ve). This Ve field reflects population-level neural activity, but does it modulate neural dynamics and the function of neural circuits? We provide a cable theory framework to study how a bundle of model neurons generates Ve and how this Ve feeds back and influences membrane potential ( Vm). We find that these “ephaptic interactions” are small but not negligible. The model neural population can generate Ve with millivolt-scale amplitude, and this Ve perturbs the Vm of “nearby” cables and effectively increases their electrotonic length. After using passive cable theory to systematically study ephaptic coupling, we explore a test case: the medial superior olive (MSO) in the auditory brain stem. The MSO is a possible locus of ephaptic interactions: sounds evoke large (millivolt scale) Ve in vivo in this nucleus. The Ve response is thought to be generated by MSO neurons that perform a known neuronal computation with submillisecond temporal precision (coincidence detection to encode sound source location). Using a biophysically based model of MSO neurons, we find millivolt-scale ephaptic interactions consistent with the passive cable theory results. These subtle membrane potential perturbations induce changes in spike initiation threshold, spike time synchrony, and time difference sensitivity. These results suggest that ephaptic coupling may influence MSO function.


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