Auditory brain stem of the ferret: some effects of rearing with a unilateral ear plug on the cochlea, cochlear nucleus, and projections to the inferior colliculus

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.

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Inferior Colliculus Responses to Multichannel Microstimulation of the Ventral Cochlear Nucleus: Implications for Auditory Brain Stem Implants

Journal of Neurophysiology ◽

10.1152/jn.00629.2007 ◽

2008 ◽

Vol 99 (1) ◽

pp. 1-13 ◽

Cited By ~ 16

Author(s):

Mohit N. Shivdasani ◽

Stefan J. Mauger ◽

Graeme D. Rathbone ◽

Antonio G. Paolini

Keyword(s):

Electrical Stimulation ◽

Brain Stem ◽

Inferior Colliculus ◽

Cochlear Nucleus ◽

Electrode Placement ◽

Ventral Cochlear Nucleus ◽

Frequency Specificity ◽

Auditory Brain Stem ◽

Acoustic Tuning ◽

Stimulation Of

Multichannel techniques were used to assess the frequency specificity of activation in the central nucleus of the inferior colliculus (CIC) produced by electrical stimulation of localized regions within the ventral cochlear nucleus (VCN). Data were recorded in response to pure tones from 141 and 193 multiunit clusters in the rat VCN and the CIC, respectively. Of 141 VCN sites, 126 were individually stimulated while recording responses in the CIC. A variety of CIC response types were seen with an increase in both electrical and acoustic stimulation levels. The majority of sites exhibited monotonic rate-level types acoustically, whereas spike rate saturation was achieved predominantly with electrical stimulation. In 20.6% of the 364 characteristic frequency aligned VCN–CIC pairs, the CIC sites did not respond to stimulation. In 26% of the 193 CIC sites, a high correlation was observed between acoustic tuning and electrical tuning obtained through VCN stimulation. A high degree of frequency specificity was found in 58% of the 118 lowest threshold VCN–CIC pairs. This was dependent on electrode placement within the VCN because a higher degree of frequency specificity was achieved with stimulation of medial, central, and posterolateral VCN regions than more anterolateral regions. Broadness of acoustic tuning in the CIC played a role in frequency-specific activation. Narrowly tuned CIC sites showed the lowest degree of frequency specificity on stimulation of the anterolateral VCN regions. These data provide significant implications for auditory brain stem implant electrode placement, current localization, power requirements, and facilitation of information transfer to higher brain centers.

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Auditory brain-stem responses evoked by electrical stimulation of the cochlear nucleus in human subjects

Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section ◽

10.1016/0168-5597(95)00022-k ◽

1995 ◽

Vol 96 (4) ◽

pp. 338-347 ◽

Cited By ~ 40

Author(s):

Michael D. Waring

Keyword(s):

Electrical Stimulation ◽

Brain Stem ◽

Cochlear Nucleus ◽

Human Subjects ◽

Auditory Brain Stem Responses ◽

Auditory Brain Stem ◽

Stimulation Of

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Refractory properties of auditory brain-stem responses evoked by electrical stimulation of human cochlear nucleus: evidence of neural generators

Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section ◽

10.1016/s0168-5597(97)00072-5 ◽

1998 ◽

Vol 108 (4) ◽

pp. 331-344 ◽

Cited By ~ 13

Author(s):

Michael D Waring

Keyword(s):

Electrical Stimulation ◽

Brain Stem ◽

Cochlear Nucleus ◽

Auditory Brain Stem Responses ◽

Auditory Brain Stem ◽

Stimulation Of

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Spike threshold adaptation diversifies neuronal operating modes in the auditory brain stem

Journal of Neurophysiology ◽

10.1152/jn.00234.2019 ◽

2019 ◽

Vol 122 (6) ◽

pp. 2576-2590

Author(s):

Susan T. Lubejko ◽

Bertrand Fontaine ◽

Sara E. Soueidan ◽

Katrina M. MacLeod

Keyword(s):

Sodium Channel ◽

Brain Stem ◽

Cochlear Nucleus ◽

Fine Tuning ◽

Threshold Dynamics ◽

Spike Threshold ◽

Operating Modes ◽

Auditory Brain Stem ◽

Spike Initiation ◽

Nucleus Angularis

Single neurons function along a spectrum of neuronal operating modes whose properties determine how the output firing activity is generated from synaptic input. The auditory brain stem contains a diversity of neurons, from pure coincidence detectors to pure integrators and those with intermediate properties. We investigated how intrinsic spike initiation mechanisms regulate neuronal operating mode in the avian cochlear nucleus. Although the neurons in one division of the avian cochlear nucleus, nucleus magnocellularis, have been studied in depth, the spike threshold dynamics of the tonically firing neurons of a second division of cochlear nucleus, nucleus angularis (NA), remained unexplained. The input-output functions of tonically firing NA neurons were interrogated with directly injected in vivo-like current stimuli during whole cell patch-clamp recordings in vitro. Increasing the amplitude of the noise fluctuations in the current stimulus enhanced the firing rates in one subset of tonically firing neurons (“differentiators”) but not another (“integrators”). We found that spike thresholds showed significantly greater adaptation and variability in the differentiator neurons. A leaky integrate-and-fire neuronal model with an adaptive spike initiation process derived from sodium channel dynamics was fit to the firing responses and could recapitulate >80% of the precise temporal firing across a range of fluctuation and mean current levels. Greater threshold adaptation explained the frequency-current curve changes due to a hyperpolarized shift in the effective adaptation voltage range and longer-lasting threshold adaptation in differentiators. The fine-tuning of the intrinsic properties of different NA neurons suggests they may have specialized roles in spectrotemporal processing. NEW & NOTEWORTHY Avian cochlear nucleus angularis (NA) neurons are responsible for encoding sound intensity for sound localization and spectrotemporal processing. An adaptive spike threshold mechanism fine-tunes a subset of repetitive-spiking neurons in NA to confer coincidence detector-like properties. A model based on sodium channel inactivation properties reproduced the activity via a hyperpolarized shift in adaptation conferring fluctuation sensitivity.

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

Journal of Neurophysiology ◽

10.1152/jn.01152.2004 ◽

2005 ◽

Vol 93 (6) ◽

pp. 3294-3312 ◽

Cited By ~ 42

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.

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Experimental Study on the Effect of Inferior Colliculus Lesions upon Auditory Brain Stem Response

International Journal of Audiology ◽

10.3109/00206098309072766 ◽

1983 ◽

Vol 22 (1) ◽

pp. 9-19 ◽

Cited By ~ 49

Author(s):

Hiroaki Funai ◽

Sotaro Funasaka

Keyword(s):

Experimental Study ◽

Brain Stem ◽

Inferior Colliculus ◽

Auditory Brain Stem Response ◽

Auditory Brain Stem ◽

Brain Stem Response

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Effects of intracochlear factors on spiral ganglion cells and auditory brain stem response after long-term electrical stimulation in deafened kittens

Otolaryngology ◽

10.1067/mhn.2000.93863 ◽

2000 ◽

Vol 122 (3) ◽

pp. 425-433

Author(s):

Eugene N. Myers ◽

Susumu Araki ◽

Atsushi Kawano ◽

H. Lee Seldon ◽

Robert K. Shepherd ◽

...

Keyword(s):

Brain Stem ◽

Inferior Colliculus ◽

Negative Correlation ◽

Volume Fraction ◽

Spiral Ganglion ◽

Organ Of Corti ◽

Scala Tympani ◽

Auditory Brain Stem Response ◽

Spiral Ganglion Cell ◽

Auditory Brain Stem

Using an animal model, we have studied the response of the auditory brain stem to cochlear implantation and the effect of intracochlear factors on this response. Neonatally, pharmacologically deafened cats (100 to more than 180 days old) were implanted with a 4-electrode array in both cochleas. Then, the left cochlea of each cat was electrically stimulated for total periods of up to 1000 hours. After a terminal 14C-2-deoxyglucose (2DG) experiment, the fraction of the right inferior colliculus with a significant accumulation of 2DG label was calculated. Using 3-dimensional computer-aided reconstruction, we examined the cochleas of these animals for spiral ganglion cell (SGC) survival and intracochlear factors such as electrode positions, degeneration of the organ of Corti, and the degree of fibrosis of the scala tympani. The distribution of each parameter was calculated along the organ of Corti from the basal end. There was a positive correlation between SGC survival and the level of fibrosis in the scala tympani, and a negative correlation between SGC survival and the degree of organ of Corti degeneration. Finally, there was a negative correlation between the 2DG-labeled inferior colliculus volume fraction and the degree of fibrosis, particularly in the 1-mm region nearest the pair of electrodes, and presumably in the basal turn.

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