Elsevier

Cognitive Brain Research

Volume 25, Issue 1, September 2005, Pages 161-168
Cognitive Brain Research

Research Report
Encoding of pitch in the human brainstem is sensitive to language experience

https://doi.org/10.1016/j.cogbrainres.2005.05.004Get rights and content

Abstract

Neural processes underlying pitch perception at the level of the cerebral cortex are influenced by language experience. We investigated whether early, pre-attentive stages of pitch processing at the level of the human brainstem may also be influenced by language experience. The human frequency following response (FFR), reflecting sustained phase-locked activity in a population of neural elements, was used to measure activity within the rostral brainstem. FFRs elicited by four Mandarin tones were recorded from native speakers of Mandarin Chinese and English. Pitch strength (reflecting robustness of neural phase-locking at the pitch periods) and accuracy of pitch tracking were extracted from the FFRs using autocorrelation algorithms. These measures revealed that the Chinese group exhibits stronger pitch representation and smoother pitch tracking than the English group. Consistent with the pitch data, FFR spectral data showed that the Chinese group exhibits stronger representation of the second harmonic relative to the English group across all four tones. These results cannot be explained by a temporal pitch encoding scheme which simply extracts the dominant interspike interval. Rather, these results support the possibility of neural plasticity at the brainstem level that is induced by language experience that may be enhancing or priming linguistically relevant features of the speech input.

Introduction

Languages that exploit variations in pitch to signal meaning differences in monosyllabic words (e.g., Mandarin Chinese: mahigh level ‘mother’, mahigh rising ‘hemp’, malow falling rising, ‘horse’, mahigh falling ‘scold’) are called tone languages. Language processing is known to be lateralized to the left hemisphere, whereas pitch perception is mediated in the right hemisphere [41]. In tone perception, cross-language behavioral [38], neuropsychological [9], and neuroimaging [10], [17] studies reveal a leftward asymmetry for native speakers of tone languages. At the cortical level, these data clearly suggest that the neural substrates of pitch perception in the processing of lexical tones are shaped by language experience. Moreover, it has also been shown that language experience may even influence basic auditory processes (e.g., pure tone perception) at the level of auditory cortex [30], [37].

This experience-dependent neural plasticity is not limited to the auditory cortex. Suga and his co-workers have demonstrated the changes in the response properties and frequency maps in the inferior colliculus of bats following auditory conditioning or focal electrical stimulation of the auditory cortex [34], [35], [36], [40]. Auditory experience of altered interaural cues for localization in young owls has been shown to produce frequency-dependent changes in interaural time difference tuning and frequency tuning of neurons in the inferior colliculus [12], [19]. In humans, a shortening of wave V latency, presumably generated in the inferior colliculus of the auditory brainstem, has been reported in a group of hearing-impaired listeners following the use of amplification as compared to no changes in wave V latency for a control group of hearing-impaired listeners who did not use amplification [27]. More directly relevant to this study are the improvements reported in encoding of the human frequency following response (FFR), the IC also being its presumed generator site, following auditory training of children with learning impairment [29]. As far as we know, it has yet to be demonstrated that neural plasticity in the FFR can be attributed to language experience.

While it is important to identify language-dependent processing systems at the cortical level, a complete understanding of the neural organization of language can only be achieved by viewing language processes as a set of computations or mappings between representations at different stages of processing [15]. In speech perception, for example, early processing stages are not to be dismissed as auditory areas and not relevant to language processing. Rather, early stages of processing on the input side may perform computations on the acoustic data that are relevant to linguistic as well as non-linguistic auditory perception. The degree of linguistic specificity is yet to be determined for computations performed at the level of the auditory brainstem.

The fact that the primary acoustic correlate of lexical tone is voice fundamental frequency (F0) [8] provides a window for exploring processing of the same acoustic parameter at two different stages of the language processing system. It is well-known that discharge periodicities and interspike intervals related to F0 are present in the responses of auditory nerve fibers [25], [26]. Neural phase-locking related to F0 plays a dominant role in the encoding of low pitch associated with complex sounds [4]. The scalp-recorded human FFR reflects sustained phase-locked activity in a population of neural elements within the rostral brainstem [11], [24], [32]. It has been demonstrated that the human FFR preserves certain spectrum-relevant information of speech sounds [6], [7], [20], [21], [22], [28], and moreover, pitch-relevant information about complex sounds that yield time-invariant pitch [13]. This pitch-relevant neural activity appears to be based on the temporal pattern of neural activity in the brainstem and not simply a reflection of neural synchronization to waveform envelope modulation pattern [14]. Indeed, the human FFR has been shown to be sufficiently dynamic to encode time-varying pitch of the four lexical tones of Mandarin Chinese [23].

The aim of this cross-language FFR study is to determine whether pitch encoding at the brainstem level is language-dependent in its response properties. FFRs are elicited in response to the four Mandarin tones. By comparing native speakers of a tone language (Mandarin) to those of a non-tone language (English), we are able to determine the extent to which these response properties (pitch strength, tracking accuracy) are sensitive to language experience.

Section snippets

Subjects

Fourteen adult native speakers of Mandarin and 13 native speakers of American English, ranging in age from 21 to 27 years, participated in the study. All Chinese subjects were born and raised in mainland China and classified as late Mandarin–English bilinguals, not having received formal instruction in English until the age of 11. They all resided in the USA for at least 1 but not more than 4 years. Hearing sensitivity in all subjects was better than 15 dB HL for octave frequencies from 500 to

Representation of voice pitch

Short-term autocorrelation functions and the running autocorrelograms of the FFR to the Tone 2 stimulus (yi2) are shown in Fig. 2 for the Chinese and English groups. In the autocorrelation functions (left panels), a peak at the fundamental period 1/F0 is observed for both groups, which means that phase-locked activity to the fundamental period is present regardless of language experience. However, the peak for the English group is smaller and broader relative to the Chinese group, suggesting

Representation of voice pitch

The major finding of this study is that greater pitch strength and more accurate pitch tracking of linguistically relevant pitch contours occur at the level of the auditory brainstem for native listeners of a tone language as compared to non-native listeners. In terms of the temporal pattern of neural activity, this means that the degree of phase-locking is greater and the variability is smaller around the phase-locked interval for the Chinese listeners compared to the English listeners.

Conclusions

The scalp-recorded FFR provides a non-invasive window to view neural processing of voice pitch in human speech sounds at the level of the auditory brainstem. Our findings demonstrate that experience-driven adaptive neural mechanisms are involved subcortically that sharpen response properties of neurons tuned for processing pitch contours that are of special relevance to a particular language. From the perspective of auditory neuroethology, this adjustment in processing pitch contours of

Acknowledgments

This research was supported in part by research grants to JG from the National Institutes of Health (R01 DC04584-04) and the Purdue Research Foundation.

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