Musical experience shapes human brainstem encoding of linguistic pitch patterns

Abstract

Music and speech are very cognitively demanding auditory phenomena generally attributed to cortical rather than subcortical circuitry. We examined brainstem encoding of linguistic pitch and found that musicians show more robust and faithful encoding compared with nonmusicians. These results not only implicate a common subcortical manifestation for two presumed cortical functions, but also a possible reciprocity of corticofugal speech and music tuning, providing neurophysiological explanations for musicians' higher language-learning ability.Both music and spoken language involve the use of functionally and acoustically complex sound and are generally attributed to the neocortex [1][2][3][4] . Less is known about how long-term experience using these complex sounds shapes subcortical circuitry and the context specificity and reciprocity of this tuning 5 . By measuring the frequency following response (FFR), which presumably originates from the auditory brainstem (inferior colliculus) and encodes the energy of the stimulus fundamental frequency (f 0 ) with high fidelity 6 , previous work 7 has found increased linguistic pitch pattern encoding in Mandarin-speaking subjects relative to English-speaking subjects. These results reflect Mandarin-speaking subjects' long-term exposure to linguistic pitch patterns, as Mandarin Chinese, a tone language, uses pitch to signal word meaning (for example, /ma/ spoken with high or rising pitch patterns means 'mother' or 'numb', respectively). Moreover, similar to research on short-term perceptual learning 8 , these results can be viewed as context specific (that is, linguistic experiences, subserved by the cortex, enhance the encoding of linguistic information at the Correspondence should be addressed to P.C.M.W. (pwong@northwestern.edu). 5 These authors contributed equally to this work.Note: Supplementary information is available on the Nature Neuroscience website. COMPETING INTERESTS STATEMENTThe authors declare no competing financial interests. Author Manuscript brainstem). The nonspecificity of this long-term usage effect, though largely unknown, is both theoretically interesting and clinically and educationally relevant. Nonspecificity would suggest that either speech-or music-related experience can tune sensory encoding in the auditory brainstem via the corticofugal pathway. Notably, this tuning, whether speech-or music-induced, would enhance all relevant auditory functions (both speech and music) subserved by the rostral brainstem. HHS Public AccessWe measured FFR responses to linguistic pitch patterns at the rostral brainstem in ten amateur musicians and ten nonmusicians who had no previous exposure to a tone language (see Supplementary Table 1 online). Musicians (instrumentalists) had at least 6 years of continuous musical training (mean = 10.7 years) starting at or before the age of 12.Nonmusicians had nomore than3 years (mean = 1.2 years) at any time in their life. Informed written consent was obtained from all subjects. While watching a video, subjects listened...

Selective neurophysiologic responses to music in instrumentalists with different listening biographies

“…One mechanism involves specialized neurons that are tuned to relevant aspects of sensory input, or attenuate irrelevant aspects [e.g., Gordon and O'Neil, 2000;Rauschecker et al, 1995;Wong et al, 2007b]. In the auditory system, which subserves both speech and music processing, evidence suggests that low-level neurons are tuned to basic acoustic properties such as center frequency (CF) and frequency modulation (FM) (''information-bearing elements'' or IBEs), while high-level neurons are sensitive to relevant parts and combinations of IBEs, which carry species-specific communicative functions [Suga, 1995;Suga et al, 2000].…”

Musicians have enhanced subcortical auditory and audiovisual processing of speech and music

“…Over the past decade, an increasing number of scientists have sought to understand what underlies this seemingly ubiquitous benefit of musical training. We now know that the musician's brain has functional adaptations for processing pitch and timbre (3)(4)(5)(6) as well as structural specializations in auditory, visual, motor, and cerebellar regions of the brain (7)(8)(9). Some studies also suggest that the interplay between modalities is stronger in musicians (10) and, in the case of conductors, that improved audiovisual task performance is related to enhanced activity in multisensory brain areas (11).…”

“…Measurements of the speech-evoked onset response and FFR, such as peak latencies and spectral amplitudes, have been studied extensively. In addition, it has been shown that these two main features of the brainstem response are influenced by viewing phoneme articulations and auditory training (6,12,37,38), thus making these responses suitable tools for the investigation of musicianship effects.…”

Long-term music training tunes how the brain temporally binds signals from multiple senses

“…Brainstem responses in musicians relative to nonmusicians have recently been shown to be faster, larger, and more reliable when encoding the periodicity of speech and music (9,10). Importantly, the enhanced auditory processing skills transferred from music to speech (11).…”