Neural representation of pitch-relevant information at both the brainstem and cortical levels of processing is influenced by language or music experience. However, the functional roles of brainstem and cortical neural mechanisms in the hierarchical network for language processing, and how they drive and maintain experience-dependent reorganization are not known. In an effort to evaluate the possible interplay between these two levels of pitch processing, we introduce a novel electrophysiological approach to evaluate pitch-relevant neural activity at the brainstem and auditory cortex concurrently. Brainstem frequency-following responses and cortical pitch responses were recorded from participants in response to iterated rippled noise stimuli that varied in stimulus periodicity (pitch salience). A control condition using iterated rippled noise devoid of pitch was employed to ensure pitch specificity of the cortical pitch response. Neural data were compared with behavioral pitch discrimination thresholds. Results showed that magnitudes of neural responses increase systematically and that behavioral pitch discrimination improves with increasing stimulus periodicity, indicating more robust encoding for salient pitch. Absence of cortical pitch response in the control condition confirms that the cortical pitch response is specific to pitch. Behavioral pitch discrimination was better predicted by brainstem and cortical responses together as compared to each separately. The close correspondence between neural and behavioral data suggest that neural correlates of pitch salience that emerge in early, preattentive stages of processing in the brainstem may drive and maintain with high fidelity the early cortical representations of pitch. These neural representations together contain adequate information for the development of perceptual pitch salience.
Objective Listeners with sensorineural hearing loss (SNHL) typically experience reduced speech perception, which is not completely restored with amplification. This likely occurs because cochlear damage, in addition to elevating audiometric thresholds, alters the neural representation of speech transmitted to higher centers along the auditory neuroaxis. While the deleterious effects of SNHL on speech perception in humans have been well-documented using behavioral paradigms, our understanding of the neural correlates underlying these perceptual deficits remains limited. Using the scalp-recorded Frequency Following Response (FFR), the authors examine the effects of SNHL and aging on subcortical neural representation of acoustic features important for pitch and speech perception, namely the periodicity envelope (F0) and temporal fine structure (TFS) (formant structure), as reflected in the phase-locked neural activity generating the FFR. Design FFRs were obtained from 10 listeners with normal hearing (NH) and 9 listeners with mild-moderate SNHL in response to a steady-state English back vowel /u/ presented at multiple intensity levels. Use of multiple presentation levels facilitated comparisons at equal sound pressure level (SPL) and equal sensation level (SL). In a second follow-up experiment to address the effect of age on envelope and TFS representation, FFRs were obtained from 25 NH and 19 listeners with mild to moderately-severe SNHL to the same vowel stimulus presented at 80 dB SPL. Temporal waveforms, Fast Fourier Transform (FFT) and spectrograms were used to evaluate the magnitude of the phase-locked activity at F0 (periodicity envelope) and F1 (TFS). Results Neural representation of both envelope (F0) and TFS (F1) at equal SPLs was stronger in NH listeners compared to listeners with SNHL. Also, comparison of neural representation of F0 and F1 across stimulus levels expressed in SPL and SL (accounting for audibility) revealed that level-related changes in F0 and F1 magnitude were different for listeners with SNHL compared to listeners with normal hearing. Further, the degradation in subcortical neural representation was observed to persist in listeners with SNHL even when the effects of age were controlled for. Conclusions Overall, our results suggest a relatively greater degradation in the neural representation of TFS compared to periodicity envelope in individuals with SNHL. This degraded neural representation of TFS in SNHL, as reflected in the brainstem FFR, may reflect a disruption in the temporal pattern of phase-locked neural activity arising from altered tonotopic maps and/or wider filters causing poor frequency selectivity in these listeners. Lastly, while preliminary results indicate that the deleterious effects of SNHL may be greater than age-related degradation in subcortical neural representation, the lack of a balanced age-matched control group in this study does not permit us to completely rule out the effects of age on subcortical neural representation.
Voice pitch is an important information-bearing component of language that is subject to experience dependent plasticity at both early cortical and subcortical stages of processing. We’ve already demonstrated that pitch onset component (Na) of the cortical pitch response (CPR) is sensitive to flat pitch and its salience. In regards to dynamic pitch, we do not yet know whether the multiple pitch-related transient components of the CPR reflect specific temporal attributes of such stimuli. Here we examine the sensitivity of the multiple transient components of CPR to changes in pitch acceleration associated with the Mandarin high rising lexical tone. CPR responses from Chinese listeners were elicited by three citation forms varying in pitch acceleration and duration. Results showed that the pitch onset component (Na) was invariant to changes in acceleration. In contrast, Na-Pb and Pb-Nb showed a systematic increase in the interpeak latency and decrease in amplitude with increase in pitch acceleration that followed the time course of pitch change across the three stimuli. A strong correlation with pitch acceleration was observed for these two components only – a putative index of pitch-relevant neural activity associated with the more rapidly-changing portions of the pitch contour. Pc-Nc marks unambiguously the stimulus offset. We therefore propose that in the early stages of cortical sensory processing, a series of neural markers flag different temporal attributes of a dynamic pitch contour: onset of temporal regularity (Na); changes in temporal regularity between onset and offset (Na-Pb, Pb-Nb); and offset of temporal regularity (Pc-Nc). At the temporal electrode sites, the stimulus with the most gradual change in pitch acceleration evoked a rightward asymmetry. Yet within the left hemisphere, stimuli with more gradual change were indistinguishable. These findings highlight the emergence of early hemispheric preferences and their functional roles as related to sensory and cognitive properties of the stimulus.
Pitch processing at cortical and subcortical stages of processing is shaped by language experience. We recently demonstrated that specific components of the cortical pitch response (CPR) index the more rapidly-changing portions of the high rising Tone 2 of Mandarin Chinese, in addition to marking pitch onset and sound offset. In this study, we examine how language experience (Mandarin vs. English) shapes the processing of different temporal attributes of pitch reflected in the CPR components using stimuli representative of within-category variants of Tone 2. Results showed that the magnitude of CPR components (Na-Pb and Pb-Nb) and the correlation between these two components and pitch acceleration were stronger for the Chinese listeners compared to English listeners for stimuli that fell within the range of Tone 2 citation forms. Discriminant function analysis revealed that the Na-Pb component was more than twice as important as Pb-Nb in grouping listeners by language affiliation. In addition, a stronger stimulus-dependent, rightward asymmetry was observed for the Chinese group at the temporal, but not frontal, electrode sites. This finding may reflect selective recruitment of experience-dependent, pitch-specific mechanisms in right auditory cortex to extract more complex, time-varying pitch patterns. Taken together, these findings suggest that long-term language experience shapes early sensory level processing of pitch in the auditory cortex, and that the sensitivity of the CPR may vary depending on the relative linguistic importance of specific temporal attributes of dynamic pitch.
Pitch experiments aimed at evaluating temporal pitch mechanism(s) often utilize complex sounds with only unresolved harmonic components, and a low-pass noise masker to eliminate the potential contribution of audible distortion products to the pitch percept. Herein we examine how: (i) masker induced reduction of neural distortion products (difference tone: DT; and cubic difference tone: CDT) alters the representation of pitch relevant information in the brainstem; and (ii) the pitch salience is altered when distortion products are reduced and/or eliminated. Scalp recorded brainstem frequency following responses (FFR) were recorded in normal hearing individuals using a complex tone with only unresolved harmonics presented in quiet, and in the presence of a low-pass masker at SNRs of +15, +5, and −5 dB. Difference limen for F0 discrimination (F0 DL) was obtained in quiet and in the presence of low-pass noise. Magnitude of DT components (with the exception of components at F0 and 2F0), and the CDT components decreased with increasing masker level. Neural pitch strength decreased with increasing masker level for both the envelope-related (FFRENV) and spectral-related (FFRSPEC) phase-locked activity. Finally, F0 DLs increased with decreasing SNRs suggesting poorer F0 discrimination with reduction of the distortion products. Collectively, these findings support the notion that both DT and CDT, as reflected in the FFRENV and FFRSPEC, respectively, influence both the brainstem representation of pitch relevant information and the pitch salience of the complex sounds.
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