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The Journal of Neuroscience : the... Mar 2022Sound-level coding in the auditory nerve is achieved through the progressive recruitment of auditory nerve fibers (ANFs) that differ in threshold of activation and in...
Sound-level coding in the auditory nerve is achieved through the progressive recruitment of auditory nerve fibers (ANFs) that differ in threshold of activation and in the stimulus level at which the spike rate saturates. To investigate the functional state of the ANFs, the electrophysiological tests routinely used in clinics only capture the first action potentials firing in synchrony at the onset of the acoustic stimulation. Assessment of other properties (e.g., spontaneous rate and adaptation time constants) requires single-fiber recordings directly from the nerve, which for ethical reasons is not allowed in humans. By combining neuronal activity measurements at the round window and signal-processing algorithms, we constructed a peristimulus time response (PSTR), with a waveform similar to the peristimulus time histograms (PSTHs) derived from single-fiber recordings in young adult female gerbils. Simultaneous recordings of round-window PSTR and single-fiber PSTH provided models to predict the adaptation kinetics and spontaneous rate of the ANFs tuned at the PSTR probe frequency. The predictive model derived from gerbils was then validated in female mice and finally applied to humans by recording PSTRs from the auditory nerve in normal-hearing patients who underwent cerebellopontine angle surgeries. A rapid adaptation time constant of ∼3 ms and a mean spontaneous rate of ∼22 spikes/s in the 4 kHz frequency range were found. This study offers a promising diagnostic tool to map the human auditory nerve, thus opening new avenues to better understanding auditory neuropathies, tinnitus, and hyperacusis. Neural adaptation in auditory nerve fibers corresponds to the reduction in the neuronal activity to prolonged or repeated sound stimulation. For obvious ethical reasons, single-fiber recordings from the auditory nerve are not feasible in humans, creating a critical gap in extending data obtained using animal models to humans. Using electrocochleography in rodents, we inferred adaptation kinetics and spontaneous discharge rates of the auditory nerve fibers in humans. Routinely used in basic and clinical laboratories, this tool will provide a better understanding of auditory disorders such as neuropathies, tinnitus, and hyperacusis, and will help to improve hearing-aid fittings.
Topics: Acoustic Stimulation; Animals; Cochlear Nerve; Evoked Potentials, Auditory; Female; Gerbillinae; Hearing; Humans; Mice; Nerve Fibers
PubMed: 35078924
DOI: 10.1523/JNEUROSCI.0858-21.2022 -
Hearing Research Aug 2011In mammals, the initial bridge between the physical world of sound and perception of that sound is established by neurons of the spiral ganglion. The cell bodies of... (Review)
Review
In mammals, the initial bridge between the physical world of sound and perception of that sound is established by neurons of the spiral ganglion. The cell bodies of these neurons give rise to peripheral processes that contact acoustic receptors in the organ of Corti, and the central processes collect together to form the auditory nerve that projects into the brain. In order to better understand hearing at this initial stage, we need to know the following about spiral ganglion neurons: (1) their cell biology including cytoplasmic, cytoskeletal, and membrane properties, (2) their peripheral and central connections including synaptic structure; (3) the nature of their neural signaling; and (4) their capacity for plasticity and rehabilitation. In this report, we will update the progress on these topics and indicate important issues still awaiting resolution.
Topics: Animals; Auditory Cortex; Auditory Pathways; Cochlear Nerve; Cytoskeleton; Hair Cells, Auditory; Humans; Nerve Growth Factors; Nerve Regeneration; Neuronal Plasticity; Neurons; Spiral Ganglion
PubMed: 21530629
DOI: 10.1016/j.heares.2011.04.003 -
Acta Otorrinolaringologica Espanola 2015Congenital malformations and acquired lesions of the inner ear are characterised by small structural changes in this region. In recent decades, treatment options have... (Review)
Review
INTRODUCTION
Congenital malformations and acquired lesions of the inner ear are characterised by small structural changes in this region. In recent decades, treatment options have improved considerably. At the same time, there has been a great advancement in diagnostic methods, obtaining high-resolution labyrinth images. Currently, we use a 64-multislice computed tomography scanner in spiral mode (Brilliance 64 Phillips, Eindhoven, the Netherlands), with an overlap of 0.66 mm and an interval of 0.33 mm, 120 KV and 300 mA. The magnetic resonance images were taken with Signa HDxt 1.5 and 3.0 T units (GE Healthcare, Waukesha, WI, USA). We reviewed the radiological features of the lesions affecting the inner ear. They are classified as congenital (labyrinth malformation and statoacoustic nerve deficiencies) or acquired (otospongiosis, labyrinthitis, Ménière's disease, inner ear haemorrhage, intralabyrinthine schwannoma and endolymphatic sac tumour).
CONCLUSION
Magnetic resonance imaging and computed tomography play an essential role in diagnosing patients with inner ear pathology. The technique selected should be chosen depending on the clinical setting. In a generic way, tomography is the method of choice for the study of traumatic pathology or otospongiosis. When tumour or inflammatory pathology is suspected, magnetic resonance is superior. In cases of congenital malformation, both techniques are complementary.
Topics: Cochlear Nerve; Congenital Abnormalities; Cystadenoma, Papillary; Disease Progression; Ear Neoplasms; Ear, Inner; Endolymphatic Sac; Hearing Loss, Sensorineural; Humans; Labyrinth Diseases; Magnetic Resonance Imaging; Multidetector Computed Tomography; Neuroma, Acoustic; Otosclerosis
PubMed: 25312404
DOI: 10.1016/j.otorri.2014.07.002 -
Proceedings of the National Academy of... Nov 2020Sounds are processed by the ear and central auditory pathway. These processing steps are biologically complex, and many aspects of the transformation from sound...
Sounds are processed by the ear and central auditory pathway. These processing steps are biologically complex, and many aspects of the transformation from sound waveforms to cortical response remain unclear. To understand this transformation, we combined models of the auditory periphery with various encoding models to predict auditory cortical responses to natural sounds. The cochlear models ranged from detailed biophysical simulations of the cochlea and auditory nerve to simple spectrogram-like approximations of the information processing in these structures. For three different stimulus sets, we tested the capacity of these models to predict the time course of single-unit neural responses recorded in ferret primary auditory cortex. We found that simple models based on a log-spaced spectrogram with approximately logarithmic compression perform similarly to the best-performing biophysically detailed models of the auditory periphery, and more consistently well over diverse natural and synthetic sounds. Furthermore, we demonstrated that including approximations of the three categories of auditory nerve fiber in these simple models can substantially improve prediction, particularly when combined with a network encoding model. Our findings imply that the properties of the auditory periphery and central pathway may together result in a simpler than expected functional transformation from ear to cortex. Thus, much of the detailed biological complexity seen in the auditory periphery does not appear to be important for understanding the cortical representation of sound.
Topics: Acoustic Stimulation; Animals; Auditory Cortex; Auditory Pathways; Auditory Perception; Cochlea; Cochlear Nerve; Ferrets; Humans; Models, Neurological; Neurons; Sound; Speech
PubMed: 33097665
DOI: 10.1073/pnas.1922033117 -
The Journal of Neuroscience : the... May 2023Modulations in both amplitude and frequency are prevalent in natural sounds and are critical in defining their properties. Humans are exquisitely sensitive to frequency...
Modulations in both amplitude and frequency are prevalent in natural sounds and are critical in defining their properties. Humans are exquisitely sensitive to frequency modulation (FM) at the slow modulation rates and low carrier frequencies that are common in speech and music. This enhanced sensitivity to slow-rate and low-frequency FM has been widely believed to reflect precise, stimulus-driven phase locking to temporal fine structure in the auditory nerve. At faster modulation rates and/or higher carrier frequencies, FM is instead thought to be coded by coarser frequency-to-place mapping, where FM is converted to amplitude modulation (AM) via cochlear filtering. Here, we show that patterns of human FM perception that have classically been explained by limits in peripheral temporal coding are instead better accounted for by constraints in the central processing of fundamental frequency (F0) or pitch. We measured FM detection in male and female humans using harmonic complex tones with an F0 within the range of musical pitch but with resolved harmonic components that were all above the putative limits of temporal phase locking (>8 kHz). Listeners were more sensitive to slow than fast FM rates, even though all components were beyond the limits of phase locking. In contrast, AM sensitivity remained better at faster than slower rates, regardless of carrier frequency. These findings demonstrate that classic trends in human FM sensitivity, previously attributed to auditory nerve phase locking, may instead reflect the constraints of a unitary code that operates at a more central level of processing. Natural sounds involve dynamic frequency and amplitude fluctuations. Humans are particularly sensitive to frequency modulation (FM) at slow rates and low carrier frequencies, which are prevalent in speech and music. This sensitivity has been ascribed to encoding of stimulus temporal fine structure (TFS) via phase-locked auditory nerve activity. To test this long-standing theory, we measured FM sensitivity using complex tones with a low F0 but only high-frequency harmonics beyond the limits of phase locking. Dissociating the F0 from TFS showed that FM sensitivity is limited not by peripheral encoding of TFS but rather by central processing of F0, or pitch. The results suggest a unitary code for FM detection limited by more central constraints.
Topics: Male; Humans; Female; Cochlear Nerve; Cochlea; Sound; Speech; Music; Acoustic Stimulation
PubMed: 37028932
DOI: 10.1523/JNEUROSCI.0995-22.2023 -
Neural Plasticity 1999This paper outlines a taxonomy of neural pulse codes and reviews neurophysiological evidence for interspike interval-based representations for pitch and timbre in the... (Review)
Review
This paper outlines a taxonomy of neural pulse codes and reviews neurophysiological evidence for interspike interval-based representations for pitch and timbre in the auditory nerve and cochlear nucleus. Neural pulse codes can be divided into channel-based codes, temporal-pattern codes, and time-of-arrival codes. Timings of discharges in auditory nerve fibers reflect the time structure of acoustic waveforms, such that the interspike intervals that are produced precisely convey information concerning stimulus periodicities. Population-wide inter-spike interval distributions are constructed by summing together intervals from the observed responses of many single Type I auditory nerve fibers. Features in such distributions correspond closely with pitches that are heard by human listeners. The most common all-order interval present in the auditory nerve array almost invariably corresponds to the pitch frequency, whereas the relative fraction of pitch-related intervals amongst all others qualitatively corresponds to the strength of the pitch. Consequently, many diverse aspects of pitch perception are explained in terms of such temporal representations. Similar stimulus-driven temporal discharge patterns are observed in major neuronal populations of the cochlear nucleus. Population-interval distributions constitute an alternative time-domain strategy for representing sensory information that complements spatially organized sensory maps. Similar autocorrelation-like representations are possible in other sensory systems, in which neural discharges are time-locked to stimulus waveforms.
Topics: Acoustic Stimulation; Animals; Auditory Pathways; Cochlear Nerve; Humans; Nerve Fibers; Neurons; Periodicity; Pitch Perception; Reaction Time
PubMed: 10714267
DOI: 10.1155/NP.1999.147 -
Hearing Research Dec 2022Cochlear implants (CIs) provide acoustic information to implanted patients by electrically stimulating nearby auditory nerve fibers (ANFs) which then transmit the... (Comparative Study)
Comparative Study Review
Cochlear implants (CIs) provide acoustic information to implanted patients by electrically stimulating nearby auditory nerve fibers (ANFs) which then transmit the information to higher-level neural structures for further processing and interpretation. Computational models that simulate ANF responses to CI stimuli enable the exploration of the mechanisms underlying CI performance beyond the capacity of in vivo experimentation alone. However, all ANF models developed to date utilize to some extent anatomical/morphometric data, biophysical properties and/or physiological data measured in non-human animal models. This review compares response properties of the electrically stimulated auditory nerve (AN) in human listeners and different mammalian models. Properties of AN responses to single pulse stimulation, paired-pulse stimulation, and pulse-train stimulation are presented. While some AN response properties are similar between human listeners and animal models (e.g., increased AN sensitivity to single pulse stimuli with long interphase gaps), there are some significant differences. For example, the AN of most animal models is typically more sensitive to cathodic stimulation while the AN of human listeners is generally more sensitive to anodic stimulation. Additionally, there are substantial differences in the speed of recovery from neural adaptation between animal models and human listeners. Therefore, results from animal models cannot be simply translated to human listeners. Recognizing the differences in responses of the AN to electrical stimulation between humans and other mammals is an important step for creating ANF models that are more applicable to various human CI patient populations.
Topics: Animals; Humans; Cochlear Implantation; Cochlear Implants; Cochlear Nerve; Electric Stimulation; Evoked Potentials, Auditory; Mammals; Models, Animal
PubMed: 36343534
DOI: 10.1016/j.heares.2022.108643 -
Age-related Changes in Neural Coding of Envelope Cues: Peripheral Declines and Central Compensation.Neuroscience May 2019Aging listeners often experience difficulties in perceiving temporally complex acoustic cues in noisy environments. These difficulties likely have neurophysiological... (Review)
Review
Aging listeners often experience difficulties in perceiving temporally complex acoustic cues in noisy environments. These difficulties likely have neurophysiological contributors from various levels of auditory processing. Cochlear synapses between inner hair cells and auditory nerve fibers exhibit a progressive decline with age which is not reflected in the threshold audiogram. The functional consequences of this loss for the coding of suprathreshold sound remain poorly understood. Recent studies suggest that cochlear synaptopathy results in degraded representations of temporal envelope cues at the earliest levels of the auditory pathway. Central nuclei downstream of the auditory nerve exhibit a compensatory plasticity in response to this deafferentation, in the form of altered gain. This results in a modulation frequency selective increase in the representation of envelope cues at the level of the auditory midbrain and cortex. These changes may be shaped by mechanisms such as decreased inhibitory neurotransmission occurring with age across various central auditory nuclei. Altered representations of the differing temporal components of speech due to these interactions between multiple levels of the auditory pathway may contribute to the age-related difficulties hearing speech in noisy environments.
Topics: Aging; Animals; Auditory Perception; Auditory Threshold; Cochlear Nerve; Evoked Potentials, Auditory, Brain Stem; Hearing; Hearing Loss, Noise-Induced; Humans
PubMed: 30553793
DOI: 10.1016/j.neuroscience.2018.12.007 -
Upsala Journal of Medical Sciences Aug 2019For the first time the expression of the ion transport protein sodium/potassium-ATPase and its isoforms was analyzed in the human cochlea using light- and confocal...
Expression of Na/K-ATPase subunits in the human cochlea: a confocal and super-resolution microscopy study with special reference to auditory nerve excitation and cochlear implantation.
For the first time the expression of the ion transport protein sodium/potassium-ATPase and its isoforms was analyzed in the human cochlea using light- and confocal microscopy as well as super-resolution structured illumination microscopy. It may increase our understanding of its role in the propagation and processing of action potentials in the human auditory nerve and how electric nerve responses are elicited from auditory prostheses. Archival human cochlear sections were obtained from trans-cochlear surgeries. Antibodies against the Na/K-ATPase β1 isoform together with α1 and α3 were used for immunohistochemistry. An algorithm was applied to assess the expression in various domains. Na/K ATPase β1 subunit was expressed, mostly combined with the α1 isoform. Neurons expressed the β1 subunit combined with α3, while satellite glial cells expressed the α1 isoform without recognized association with β1. Types I and II spiral ganglion neurons and efferent fibers expressed the Na/K-ATPase α3 subunit. Inner hair cells, nerve fibers underneath, and efferent and afferent fibers in the organ of Corti also expressed α1. The highest activity of Na/K-ATPase β1 was at the inner hair cell/nerve junction and spiral prominence. The human auditory nerve displays distinct morphologic features represented in its molecular expression. It was found that electric signals generated via hair cells may not go uninterrupted across the spiral ganglion, but are locally processed. This may be related to particular filtering properties in the human acoustic pathway.
Topics: Acoustic Stimulation; Animals; Cochlea; Cochlear Implantation; Cochlear Nerve; Humans; Immunohistochemistry; In Vitro Techniques; Mice; Microscopy, Confocal; Microscopy, Electron, Transmission; Sodium-Potassium-Exchanging ATPase
PubMed: 31460814
DOI: 10.1080/03009734.2019.1653408 -
Journal of the Association For Research... Sep 2009Persons with a prosthesis implanted in a cochlea with residual acoustic sensitivity can, in some cases, achieve better speech perception with "hybrid" stimulation than...
Persons with a prosthesis implanted in a cochlea with residual acoustic sensitivity can, in some cases, achieve better speech perception with "hybrid" stimulation than with either acoustic or electric stimulation presented alone. Such improvements may involve "across auditory-nerve fiber" processes within central nuclei of the auditory system and within-fiber interactions at the level of the auditory nerve. Our study explored acoustic-electric interactions within feline auditory nerve fibers (ANFs) so as to address two goals. First, we sought to better understand recent results that showed non-monotonic recovery of the electrically evoked compound action potential (ECAP) following acoustic masking (Nourski et al. 2007, Hear. Res. 232:87-103). We hypothesized that post-masking changes in ANF temporal properties and responsiveness (spike rate) accounted for the ECAP results. We also sought to describe, more broadly, the changes in ANF responses that result from prior acoustic stimulation. Five response properties-spike rate, latency, jitter, spike amplitude, and spontaneous activity-were examined. Post-masking reductions in spike rate, within-fiber jitter and across-fiber variance in latency were found, with the changes in temporal response properties limited to ANFs with high spontaneous rates. Thus, our results suggest how non-monotonic ECAP recovery occurs for ears with spontaneous activity, but cannot account for that pattern of recovery when there is no spontaneous activity, including the results from the presumably deafened ears used in the Nourski et al. (2007) study. Finally, during simultaneous (electric+acoustic) stimulation, the degree of electrically driven spike activity had a strong influence on spike rate, but did not affect spike jitter, which apparently was determined by the acoustic noise stimulus or spontaneous activity.
Topics: Acoustic Stimulation; Action Potentials; Animals; Cats; Cochlear Nerve; Electric Stimulation; Evoked Potentials, Auditory; Models, Animal; Nerve Fibers
PubMed: 19205803
DOI: 10.1007/s10162-008-0154-7