On the mechanism of response latencies in auditory nerve fibers

Despite the structural differences of the middle and inner ears, the latency pattern in auditory nerve fibers to an identical sound has been found similar across numerous species. Studies have shown the similarity in remarkable species with distinct cochleae or even without a basilar membrane. This stimulus-, neuron-, and species- independent similarity of latency cannot be simply explained by the concept of cochlear traveling waves that is generally accepted as the main cause of the neural latency pattern. An original concept of Fourier pattern is defined, intended to characterize a feature of temporal processing—specifically phase encoding—that is not readily apparent in more conventional analyses. The pattern is created by marking the first amplitude maximum for each sinusoid component of the stimulus, to encode phase information. The hypothesis is that the hearing organ serves as a running analyzer whose output reflects synchronization of auditory neural activity consistent with the Fourier pattern. A combined research of experimental, correlational and meta-analysis approaches is used to test the hypothesis. Manipulations included phase encoding and stimuli to test their effects on the predicted latency pattern. Animal studies in the literature using the same stimulus were then compared to determine the degree of relationship. The results show that each marking accounts for a large percentage of a corresponding peak latency in the peristimulus-time histogram. For each of the stimuli considered, the latency predicted by the Fourier pattern is highly correlated with the observed latency in the auditory nerve fiber of representative species. The results suggest that the hearing organ analyzes not only amplitude spectrum but also phase information in Fourier analysis, to distribute the specific spikes among auditory nerve fibers and within a single unit. This phase-encoding mechanism in Fourier analysis is proposed to be the common mechanism that, in the face of species differences in peripheral auditory hardware, accounts for the considerable similarities across species in their latency-by-frequency functions, in turn assuring optimal phase encoding across species. Also, the mechanism has the potential to improve phase encoding of cochlear implants

Restoring the encoding properties of a stochastic neuron model by an exogenous noise

Here we evaluate the possibility of improving the encoding properties of an impaired neuronal system by superimposing an exogenous noise to an external electric stimulation signal. The approach is based on the use of mathematical neuron models consisting of stochastic HH-like circuit, where the impairment of the endogenous presynaptic inputs is described as a subthreshold injected current and the exogenous stimulation signal is a sinusoidal voltage perturbation across the membrane. Our results indicate that a correlated Gaussian noise, added to the sinusoidal signal can significantly increase the encoding properties of the impaired system, through the Stochastic Resonance (SR) phenomenon. These results suggest that an exogenous noise, suitably tailored, could improve the efficacy of those stimulation techniques used in neuronal systems, where the presynaptic sensory neurons are impaired and have to be artificially bypassed

Cross-Correlation in the Auditory Coincidence Detectors of Owls

Interaural time difference (ITD) plays a central role in many auditory functions, most importantly in sound localization. The classic model for how ITD is computed was put forth by Jeffress (1948). One of the predictions of the Jeffress model is that the neurons that compute ITD should behave as cross-correlators. Whereas cross-correlation-like properties of the ITD-computing neurons have been reported, attempts to show that the shape of the ITD response function is determined by the spectral tuning of the neuron, a core prediction of cross-correlation, have been unsuccessful. Using reverse correlation analysis, we demonstrate in the barn owl that the relationship between the spectral tuning and the ITD response of the ITD-computing neurons is that predicted by cross-correlation. Moreover, we show that a model of coincidence detector responses derived from responses to binaurally uncorrelated noise is consistent with binaural interaction based on cross-correlation. These results are thus consistent with one of the key tenets of the Jeffress model. Our work sets forth both the methodology to answer whether cross-correlation describes coincidence detector responses and a demonstration that in the barn owl, the result is that expected by theory

Sparse Codes for Speech Predict Spectrotemporal Receptive Fields in the Inferior Colliculus

We have developed a sparse mathematical representation of speech that minimizes the number of active model neurons needed to represent typical speech sounds. The model learns several well-known acoustic features of speech such as harmonic stacks, formants, onsets and terminations, but we also find more exotic structures in the spectrogram representation of sound such as localized checkerboard patterns and frequency-modulated excitatory subregions flanked by suppressive sidebands. Moreover, several of these novel features resemble neuronal receptive fields reported in the Inferior Colliculus (IC), as well as auditory thalamus and cortex, and our model neurons exhibit the same tradeoff in spectrotemporal resolution as has been observed in IC. To our knowledge, this is the first demonstration that receptive fields of neurons in the ascending mammalian auditory pathway beyond the auditory nerve can be predicted based on coding principles and the statistical properties of recorded sounds.Comment: For Supporting Information, see PLoS website: http://www.ploscompbiol.org/article/info%3Adoi%2F10.1371%2Fjournal.pcbi.100259

Sodium-activated potassium channels shape peripheral auditory function and activity of the primary auditory neurons in mice

Potassium (K+) channels shape the response properties of neurons. Although enormous progress has been made to characterize K+ channels in the primary auditory neurons, the molecular identities of many of these channels and their contributions to hearing in vivo remain unknown. Using a combination of RNA sequencing and single molecule fluorescent in situ hybridization, we localized expression of transcripts encoding the sodium-activated potassium channels K(Na)1.1(SLO2.2/Slack) and K(Na)1.2 (SLO2.1/Slick) to the primary auditory neurons (spiral ganglion neurons, SGNs). To examine the contribution of these channels to function of the SGNs in vivo, we measured auditory brainstem responses in K(Na)1.1/1.2 double knockout (DKO) mice. Although auditory brainstem response (wave I) thresholds were not altered, the amplitudes of suprathreshold responses were reduced in DKO mice. This reduction in amplitude occurred despite normal numbers and molecular architecture of the SGNs and their synapses with the inner hair cells. Patch clamp electrophysiology of SGNs isolated from DKO mice displayed altered membrane properties, including reduced action potential thresholds and amplitudes. These findings show that K(Na)1 channel activity is essential for normal cochlear function and suggest that early forms of hearing loss may result from physiological changes in the activity of the primary auditory neurons

Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier.

The dynamic adjustment of hearing sensitivity and frequency selectivity is mediated by the medial olivocochlear efferent reflex, which suppresses the gain of the 'cochlear amplifier' in each ear. Such efferent feedback is important for promoting discrimination of sounds in background noise, sound localization and protecting the cochleae from acoustic overstimulation. However, the sensory driver for the olivocochlear reflex is unknown. Here, we resolve this longstanding question using a mouse model null for the gene encoding the type III intermediate filament peripherin (Prph). Prph((-/-)) mice lacked type II spiral ganglion neuron innervation of the outer hair cells, whereas innervation of the inner hair cells by type I spiral ganglion neurons was normal. Compared with Prph((+/+)) controls, both contralateral and ipsilateral olivocochlear efferent-mediated suppression of the cochlear amplifier were absent in Prph((-/-)) mice, demonstrating that outer hair cells and their type II afferents constitute the sensory drive for the olivocochlear efferent reflex

Temporal modulation transfer functions in the European Starling (Sturnus vulgaris): II. Responses of auditory-nerve fibres

The temporal resolution of cochlear-nerve fibres in the European starling was determined with sinusoidally amplitude-modulated noise stimuli similar to those previously used in a psychoacoustic study in this species (Klump and Okanoya, 1991). Temporal modulation transfer curves (TMTFs) were constructed for cochlear afferents allowing a direct comparison with the starling's behavioural performance. On average, the neuron's detection of modulation was less sensitive than that obtained in the behavioural experiments, although the most sensitive cells approached the values determined psychophysically. The shapes of the neural TMTFs generally resembled low-pass or band-pass filter functions, and the shapes of the averaged neural functions were very similar to those obtained in the behavioural study for two different types of stimuli (gated and continuous carrier). Minimum integration times calculated from the upper cut-off frequency of the neural TMTFs had a median of 0.97 ms with a range of 0.25 to 15.9 ms. The relations between the minimum integration times and the tuning characteristics of the cells (tuning curve bandwidth, Q10 dB-value, high- and low-frequency slopes of the tuning curves) are discussed. Finally, we compare the TMTF data recorded in the starling auditory nerve with data from neurophysiological and behavioural observations on temporal resolution using other experimental paradigms in this and other vertebrate species