Neural Temporal Coding Research Articles

Subclinical Auditory Neural Deficits in Patients With Type 1 Diabetes Mellitus

Diabetes mellitus (DM) is associated with a variety of sensory complications. Very little attention has been given to auditory neuropathic complications in DM. The aim of this study was to determine whether type 1 DM (T1DM) affects neural coding of the rapid temporal fluctuations of sounds, and how any deficits may impact on behavioral performance. Participants were 30 young normal-hearing T1DM patients, and 30 age-, sex-, and audiogram-matched healthy controls. Measurements included electrophysiological measures of auditory nerve and brainstem function using the click-evoked auditory brainstem response, and of brainstem neural temporal coding using the sustained frequency-following response (FFR); behavioral tests of temporal coding (interaural phase difference discrimination and the frequency difference limen); tests of speech perception in noise; and self-report measures of auditory disability using the Speech, Spatial and Qualities of Hearing Scale. There were no significant differences between T1DM patients and controls in the auditory brainstem response. However, the T1DM group showed significantly reduced FFRs to both temporal envelope and temporal fine structure. The T1DM group also showed significantly higher interaural phase difference and frequency difference limen thresholds, worse speech-in-noise performance, as well as lower overall Speech, Spatial and Qualities scores than the control group. These findings suggest that T1DM is associated with degraded neural temporal coding in the brainstem in the absence of an elevation in audiometric threshold, and that the FFR may provide an early indicator of neural damage in T1DM, before any abnormalities can be identified using standard clinical tests. However, the relation between the neural deficits and the behavioral deficits is uncertain.

Neural ITD Sensitivity and Temporal Coding with Cochlear Implants in an Animal Model of Early-Onset Deafness.

Users of cochlear implant (CI) face challenges in everyday situations such as understanding conversations in noise, even with CIs in both ears. These challenges are related to difficulties with tasks that require fine temporal processing such as discrimination of pulse rates or interaural time differences (ITD), a major cue for sound localization. The degradation in temporal processing and ITD sensitivity are especially acute in those who lost hearing in early childhood. Here, we characterized temporal coding and ITD sensitivity of single neurons in a novel animal model of early-onset deafness. Rabbits were deafened as neonates and deprived of auditory stimulation until they reached adult age when single-unit recordings from the auditory midbrain were made chronically using an unanesthetized preparation. The results are compared to measurements from adult-deafened rabbits with normal auditory development to understand the effect of early-onset deafness on neural temporal coding and ITD sensitivity. Neurons in the inferior colliculus (IC) of early-deafened rabbits were less likely to show sustained, excitatory responses to pulse train stimulation and more likely to show suppressive responses compared to neurons in adult-deaf animals. Fewer neurons showed synchronized responses to pulse trains at any rate in the early-deaf group. In addition, fewer neurons showed significant ITD sensitivity in their overall firing rate in the early-deaf group compared to adult-deaf animals. Neural ITD discrimination thresholds in the early-deaf group were poorer than thresholds in adult-deaf group, especially at high pulse rates. The overall degradation in neural ITD sensitivity is consistent with the difficulties encountered by human CI users with early-onset hearing loss. These results lay the groundwork for investigating whether the degradations in temporal coding and ITD sensitivity observed in early-deaf animals can be reversed by appropriate CI stimulation during development.

Sub-clinical auditory neural deficits in patients with type 1 Diabetes Mellitus

Diabetes mellitus (DM) is associated with a variety of sensory complications. Very little attention has been given to auditory neuropathic complications in DM. The aim of this study was to determine whether type 1 DM affects neural coding of the rapid temporal fluctuations of sounds, and how any deficits may impact on real-world listening tasks. Participants were 30young normal-hearing type 1 DM patients, and 30 age-, sex-, and audiogram-matched healthy controls. Tests included non-invasive electrophysiological measures of auditory nerve and brainstem function using the click-evoked auditory brainstem response (ABR), and of brainstem neural temporal coding using the sustained frequency-following response (FFR), as well as behavioural tests of temporal coding (interaural phase difference, IPD, discrimination and the frequency difference limen, FDL) and tests of speech perception in noise. There were no significant differences between DM patients and controls in the ABR. However, the DM group showed significantly lower FFR responses, higher IPD and FDL thresholds, as well as worse speech-in-noise performance. The results suggest that type 1 DM is associated with degraded neural temporal coding in the brainstem in the absence of an elevation in audiometric threshold, and that this deficit may impact on real-world hearing ability.

Differential effects of noise trauma and diminished endocochlear potential on neural temporal coding of complex sounds: Implications for speech perception

Communication problems due to cochlear hearing loss are pervasive in today’s society, even with amplification from digital hearing aids. Threshold elevation may arise from noise-induced trauma to hair cells or, as an alternative mechanism, through age-related depletion of the endocochlear potential (EP; the power supply driving hair-cell function). While both noise trauma and diminished EP may frequently underlie hearing loss in older people, it is unclear whether these pathologies have different effects on neural coding of complex sounds, and ultimately, on speech perception. Here, we describe several recent neurophysiological studies of this question based on Wiener-kernel analyses of chinchilla auditory-nerve fiber responses to Gaussian noise. We find that noise trauma causes pronounced distortions in tonotopic coding of temporal fine structure and slower envelope cues, occurring with as little as 20 dB threshold elevation. Similar changes in neural coding occur with diminished EP, but only when thresh...

Losing the music: aging affects the perception and subcortical neural representation of musical harmony.

When two musical notes with simple frequency ratios are played simultaneously, the resulting musical chord is pleasing and evokes a sense of resolution or "consonance". Complex frequency ratios, on the other hand, evoke feelings of tension or "dissonance". Consonance and dissonance form the basis of harmony, a central component of Western music. In earlier work, we provided evidence that consonance perception is based on neural temporal coding in the brainstem (Bones et al., 2014). Here, we show that for listeners with clinically normal hearing, aging is associated with a decline in both the perceptual distinction and the distinctiveness of the neural representations of different categories of two-note chords. Compared with younger listeners, older listeners rated consonant chords as less pleasant and dissonant chords as more pleasant. Older listeners also had less distinct neural representations of consonant and dissonant chords as measured using a Neural Consonance Index derived from the electrophysiological "frequency-following response." The results withstood a control for the effect of age on general affect, suggesting that different mechanisms are responsible for the perceived pleasantness of musical chords and affective voices and that, for listeners with clinically normal hearing, age-related differences in consonance perception are likely to be related to differences in neural temporal coding.

Subcortical representation of musical dyads: Individual differences and neural generators

When two notes are played simultaneously they form a musical dyad. The sensation of pleasantness, or “consonance”, of a dyad is likely driven by the harmonic relation of the frequency components of the combined spectrum of the two notes. Previous work has demonstrated a relation between individual preference for consonant over dissonant dyads, and the strength of neural temporal coding of the harmonicity of consonant relative to dissonant dyads as measured using the electrophysiological “frequency-following response” (FFR). However, this work also demonstrated that both these variables correlate strongly with musical experience. The current study was designed to determine whether the relation between consonance preference and neural temporal coding is maintained when controlling for musical experience. The results demonstrate that strength of neural coding of harmonicity is predictive of individual preference for consonance even for non-musicians. An additional purpose of the current study was to assess the cochlear generation site of the FFR to low-frequency dyads. By comparing the reduction in FFR strength when high-pass masking noise was added to the output of a model of the auditory periphery, the results provide evidence for the FFR to low-frequency dyads resulting in part from basal cochlear generators.

Phase locked neural activity in the human brainstem predicts preference for musical consonance

When musical notes are combined to make a chord, the closeness of fit of the combined spectrum to a single harmonic series (the ‘harmonicity’ of the chord) predicts the perceived consonance (how pleasant and stable the chord sounds; McDermott, Lehr, & Oxenham, 2010). The distinction between consonance and dissonance is central to Western musical form. Harmonicity is represented in the temporal firing patterns of populations of brainstem neurons. The current study investigates the role of brainstem temporal coding of harmonicity in the perception of consonance. Individual preference for consonant over dissonant chords was measured using a rating scale for pairs of simultaneous notes. In order to investigate the effects of cochlear interactions, notes were presented in two ways: both notes to both ears or each note to different ears. The electrophysiological frequency following response (FFR), reflecting sustained neural activity in the brainstem synchronised to the stimulus, was also measured. When both notes were presented to both ears the perceptual distinction between consonant and dissonant chords was stronger than when the notes were presented to different ears. In the condition in which both notes were presented to the both ears additional low-frequency components, corresponding to difference tones resulting from nonlinear cochlear processing, were observable in the FFR effectively enhancing the neural harmonicity of consonant chords but not dissonant chords. Suppressing the cochlear envelope component of the FFR also suppressed the additional frequency components. This suggests that, in the case of consonant chords, difference tones generated by interactions between notes in the cochlea enhance the perception of consonance. Furthermore, individuals with a greater distinction between consonant and dissonant chords in the FFR to individual harmonics had a stronger preference for consonant over dissonant chords. Overall, the results provide compelling evidence for the role of neural temporal coding in the perception of consonance, and suggest that the representation of harmonicity in phase locked neural firing drives the perception of consonance.

Effects of estrogen augmentation on cognition and symptoms in female schizophrenia patients

When musical notes are combined to make a chord, the closeness of fit of the combined spectrum to a single harmonic series (the ‘harmonicity’ of the chord) predicts the perceived consonance (how pleasant and stable the chord sounds; McDermott, Lehr, & Oxenham, 2010). The distinction between consonance and dissonance is central to Western musical form. Harmonicity is represented in the temporal firing patterns of populations of brainstem neurons. The current study investigates the role of brainstem temporal coding of harmonicity in the perception of consonance. Individual preference for consonant over dissonant chords was measured using a rating scale for pairs of simultaneous notes. In order to investigate the effects of cochlear interactions, notes were presented in two ways: both notes to both ears or each note to different ears. The electrophysiological frequency following response (FFR), reflecting sustained neural activity in the brainstem synchronised to the stimulus, was also measured. When both notes were presented to both ears the perceptual distinction between consonant and dissonant chords was stronger than when the notes were presented to different ears. In the condition in which both notes were presented to the both ears additional low-frequency components, corresponding to difference tones resulting from nonlinear cochlear processing, were observable in the FFR effectively enhancing the neural harmonicity of consonant chords but not dissonant chords. Suppressing the cochlear envelope component of the FFR also suppressed the additional frequency components. This suggests that, in the case of consonant chords, difference tones generated by interactions between notes in the cochlea enhance the perception of consonance. Furthermore, individuals with a greater distinction between consonant and dissonant chords in the FFR to individual harmonics had a stronger preference for consonant over dissonant chords. Overall, the results provide compelling evidence for the role of neural temporal coding in the perception of consonance, and suggest that the representation of harmonicity in phase locked neural firing drives the perception of consonance.

Neural temporal coding of low pitch. I. Human frequency-following responses to complex tones

The neural basis of low pitch was investigated in the present study by recording a brainstem potential from the scalp of human subjects during presentation of complex tones which evoke a variable sensation of pitch. The potential recorded, the frequency-following response (FFR), reflects the temporal discharge activity of auditory neurons in the upper brainstem pathway. It was used as an index of neural periodicity in order to determine the extent to which the low pitch of complex tones is encoded in the temporal discharge activity of auditory brainstem neurons. A tone composed of harmonics of a common fundamental produces a sensation of pitch equal to that of the ‘missing’ fundamental. Such signals generate brainstem potentials which are spectrally similar to FFR recorded in response to sinusoidal signals equal in frequency to the missing fundamental. Both types of signals generate FFR which are periodic, with a frequency similar to the perceived pitch of the stimuli. It is shown that the FFR to the missing fundamental is not the result of a distortion product by recording FFR to a complex signal in the presence of low-frequency bandpass noise. Neither is the FFR the result of neural synchronization to the waveform envelope modulation pattern. This was determined by recording FFR to inharmonic and quasi-frequency-modulated signals. It was also determined that the ‘existence region’ for FFR to the missing fundamental lies below 2 kHz and that the most favorable spectral region for FFR to complex tones is between 0.5 and 1.0 kHz. These results are consistent with the hypothesis that far-field-recorded FFR does reflect neural activity germane to the processing of low pitch and that such pitch-relevant activity is based on the temporal discharge patterns of neurons in the upper auditory brainstem pathway.