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Subcortical processing of speech regularities underlies reading and music aptitude in children

Subcortical processing of speech regularities underlies reading and music aptitude in children Background: Neural sensitivity to acoustic regularities supports fundamental human behaviors such as hearing in noise and reading. Although the failure to encode acoustic regularities in ongoing speech has been associated with language and literacy deficits, how auditory expertise, such as the expertise that is associated with musical skill, relates to the brainstem processing of speech regularities is unknown. An association between musical skill and neural sensitivity to acoustic regularities would not be surprising given the importance of repetition and regularity in music. Here, we aimed to define relationships between the subcortical processing of speech regularities, music aptitude, and reading abilities in children with and without reading impairment. We hypothesized that, in combination with auditory cognitive abilities, neural sensitivity to regularities in ongoing speech provides a common biological mechanism underlying the development of music and reading abilities. Methods: We assessed auditory working memory and attention, music aptitude, reading ability, and neural sensitivity to acoustic regularities in 42 school-aged children with a wide range of reading ability. Neural sensitivity to acoustic regularities was assessed by recording brainstem responses to the same speech sound presented in predictable and variable speech streams. Results: Through correlation analyses and structural equation modeling, we reveal that music aptitude and literacy both relate to the extent of subcortical adaptation to regularities in ongoing speech as well as with auditory working memory and attention. Relationships between music and speech processing are specifically driven by performance on a musical rhythm task, underscoring the importance of rhythmic regularity for both language and music. Conclusions: These data indicate common brain mechanisms underlying reading and music abilities that relate to how the nervous system responds to regularities in auditory input. Definition of common biological underpinnings for music and reading supports the usefulness of music for promoting child literacy, with the potential to improve reading remediation. The human nervous system makes use of sensory regula- regularly-occurring, as opposed to unpredictably-occur- rities to drive accurate perception, especially when con- ring, stimuli [3-5]. The brain’s ability to use sensory regu- fronted with challenging perceptual environments [1]. It larities is a fundamental feature of auditory processing, is thought that the brain shapes perception according to promoting even the most basic of auditory experiences predictions that are made based on regularities; this such as language processing during infancy [6,7] and shaping is accomplished by comparing higher-level pre- speech comprehension amidst a competing conversa- tional background [5]. Failure of the brain to utilize dictions with lower-level sensory encoding of an incom- ing stimulus via the corticofugal (i.e., top down) system sensory regularities has been associated with neural dys- [2]. This is a common neural feature that spans sensory function, such as schizophrenia [8] and language impair- modalities and can be observed in neural responses to ment (e.g., dyslexia) [5,9-11]. The impact of stimulus regularity on auditory proces- sing has been well established in the auditory cortex [1,3] * Correspondence: nkraus@northwestern.edu Auditory Neuroscience Laboratory, Northwestern University, Evanston, IL, and was recently documented at and below the level of USA the brainstem [12-15]. Specifically, neural potentials to Full list of author information is available at the end of the article © 2011 Strait et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 2 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 frequently-occurring sounds exhibit enhanced frequency biological underpinnings for music and reading abilities. tuning in both the primary auditory cortex [16] and in We anticipated that music aptitude and literacy abilities the auditory brainstem [5,17]. This sensory fine-tuning would positively correlate with subcortical spectral occurs rapidly, does not require overt attention and may enhancement of repetitive speech cues. We also explored enable enhanced object discrimination [14,18]. Although relationships between musical skill and literacy-related reference to the neural enhancement of a repeated aspects of auditory cognitive function through working memory assessments [35,36], which included an auditory speech sound might seem contradictory to the well- attention component. We anticipated that music aptitude known repetition suppression of cortical evoked response and literacy abilities would positively correlate with audi- magnitudes, the neural mechanisms underlying this effect remain debated. While some have proposed that stimulus tory working memory and attention performance. In repetition leads to overall decreased neuronal activity, order to delineate and quantify relationships among vari- others have suggested that repetition facilitates precision ables, we applied the data to Structural Equation Model- in neural representation by enhancing certain aspects of ing (SEM). SEM relies on a variety of simultaneous the neural response while inhibiting others (e.g., more statistical methods (e.g., factor analysis, multiple regres- precise inhibitory sidebands surrounding a facilitated sions and path analysis combined with structural equa- response to the physical dimensions of a repeated stimu- tion relations) to evaluate a hypothesized model [37]. lus) [4]. Although more traditional regression analyses are useful Human auditory brainstem responses (ABRs) to the for delineating causal relationships among variables, SEM pitch of predictably presented speech are enhanced rela- enables more efficient characterization of complex, real- tive to ABRs to speech presented in a variable context world processes than can be achieved using correlation- [5]. The extent of this subcortical enhancement of regu- based analyses [38]. Specific benefits of SEM include the larly-occurring speech relates to better performance on simultaneous analysis of multiple interrelated variables, language-related tasks, such as reading and hearing consideration of measurement error, and inherent con- speech in noise. This fine-tuning is thought to be driven trol for multiple comparisons. We expected SEM to sub- by top-down cortical modulation of subcortical response stantiate our hypothesis that music aptitude predicts properties [19] and its absence in poor readers is consis- much of the variance in literacy abilities by way of shared tent with proposals that child reading impairment stems cognitive and neural mechanisms. from the brain’s inability to benefit from repetition in the sensory stream. Specifically, children with dyslexia fail to Materials and methods form perceptual anchors–a type of perceptual memory– Participants based on repeating sounds [9,11]. 42 normal hearing children between the ages of 8-13 Although we have made gains in understanding the years (M = 10.4, SD = 1.6, Males = 26). Participants and auditory processing of speech regularities in children their legal guardians provided informed assent and con- with reading impairment (or lack thereof), we do not sent according to Northwestern University’s Institutional know how auditory expertise shapes these mechanisms. Review Board. Because we aimed to evaluate neural func- The auditory expertise engendered by musical training tion and music aptitude across a spectrum of readers, no during childhood and into adulthood promotes the sub- literacy restrictions were applied but all participants cortical encoding of speech [20,21] and may strengthen demonstrated normal audiometric thresholds (≤20 dB neural mechanisms that undergird child literacy [22-24]. HL pure tone thresholds at octave frequencies from 125 Although the integrative nature of music and language to 8000 Hz) and IQ (≥85 score on the Wechsler Abbre- abilities continues to be debated [25-27], a growing body viated Scale of Intelligence) [39]. Participants also had of work supports shared abilities for music and reading, clinically normal ABRs to 80 dB SPL 100 μs click stimuli with music aptitude accounting for a substantial amount that were presented at 31.1 Hz. of the variance in child reading ability [28-30] even after Extent of extracurricular activity was assessed by a par- controlling for nonverbal IQ and phonological awareness ent questionnaire (the Child Behavior Checklist [40]). Par- [31]. It is thought that strengthened top-down control, ents rated their child’s current extracurricular activities which is important for modulating lower-level neural according to the frequency of the child’s involvement–less responses, unfolds with expertise [32] and, more specifi- than average, average, or more than average; these scores cally, with musical training [33,34]. were summed to produce a single extracurricular activity In order to define relationships between musical skill score. and literacy-related aspects of auditory brainstem func- Good (n = 8) and poor readers (n = 21) were differen- tion, we assessed subcortical processing of speech regula- tiated based on reading ability (Test of Word Reading rities, music aptitude and reading abilities in school-aged Efficiency; see Reading and working memory,below) [5]. children. Our overarching goal was to define common Children with scores ≤90 were included in the poor Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 3 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 reading group, while good readers had scores ≥110. 13 musical sound and compare two sequentially presented subjects did not meet the criteria for either group and sound patterns. Tonal aptitude was assessed by the were excluded from group analyses. Good and poor read- Tonal subtest, in which participants are presented with ers did not differ in age (Mann-Whitney U test; z = 40 pairs of musical excerpts that do not differ rhythmi- -0.223, p = 0.83), sex (Pearson Chi-Square c =0.12, p= cally but may differ melodically. Rhythm aptitude was 0.73), socioeconomic status as inferred by maternal edu- assessed by the Rhythm subtest, in which participants cation [41] (Pearson Chi-Square c = 1.10, p = 0.59), are presented with 40 pairs of short excerpts that do years of musical training (Mann-Whitney U test; z = not differ melodically but may differ rhythmically. For -0.231, p = 0.82), extent of extracurricular activity both subtests, participants indicate whether the two (Mann-Whitney U test; z = -1.202, p = 0.23) or nonverbal excerpts in each pair are the same or different. The IQ (Mann-Whitney U test; z = -1.834, p = 0.07). With subtest scores are combined to generate a composite regard to musical training histories, 36 of the 42 children music aptitude score. The rhythm, tonal and composite had undergone no to only a few months of musical train- scores are normed by academic grade in order to pro- ing and were not currently involved in music activities. duce percentile rankings. The other six children had participated in at least one year of musical training. One of these children was cate- Auditory brainstem measures gorized as a poor reader, two were categorized as good Brainstem responses to the speech sound /da/ were col- readers and three were considered average readers (as lected from Cz using Scan 4.3 (Compumedics, Charlotte, such, these three were not included in either reading NC) under two conditions. Ag-AgCl electrodes were group). applied in a vertical, ipsilateral montage (i.e., FPz as ground, right earlobe as reference). Evoked potentials Reading and working memory recorded with this electrode montage have been found to Standardized literacy measures assessed oral (Test of reflect activity from an ensemble of neural elements of Word Reading Efficiency, TOWRE) [42] and silent (Test central brainstem origin [48,49]. In the predictable condi- of Silent Word Reading Fluency, TOSWRF) [43] reading tion, the speech sound /da/ was presented at a probability speed. The TOWRE requires children to read aloud lists of 100%, whereas in the variable condition /da/ was ran- of real words (Sight subtest) and nonsense words (Phone- domly interspersed in the context of seven other speech mic Decoding subtest) while being timed. The two sub- sounds at a probability of 13% (Figure 1). The seven scores are combined to form a composite score (here speech sounds varied acoustically according to a variety referred to as the TOWRE). The TOSWRF requires parti- of features, including formant structure (/ba/, /ga/, /du/), cipants to quickly identify printed words by demarcating duration (a 163 ms /da/), voice-onset-time (/ta/) and F lines of letters into individual words while being timed. (250 Hz /da/, /da/ with a dipping pitch contour). The Participants are presented with rows of words that gradu- /da/ stimulus was a six-formant, 170 ms speech syllable ally increase in reading difficulty and they are asked to synthesized in Klatt [50] with a 5 ms voice onset time separate them (e.g., dimhowfigblue ® dim/how/fig/blue). and a level fundamental frequency (F , 100 Hz). The first, TOWRE ("reading efficiency”) and TOSWRF ("reading flu- second and third formants were dynamic over the first 50 ency”) age-normed scores were averaged in order to create ms (F , 400-720 Hz; F , 1700-1240 Hz; F , 2580-2500 Hz) 1 2 3 a composite Reading variable for correlation analyses. and then maintained frequency for the rest of the dura- Auditory working memory was assessed using the tion. The fourth, fifth and sixth formants were constant Memory for Digits Forward subtest of the Comprehen- throughout the entire duration of the stimulus (F , 3300 sive Test of Phonological Processing [44] and the Mem- Hz; F ,3750Hz; F , 4900 Hz). For a detailed description 5 6 ory for Digits Reversed subtest of the Woodcock Johnson of the seven other speech sounds, see Chandrasekaran Test of Cognitive Abilities [45]. Digits forward and digits et al. (2009). reversed age-normed scores were averaged in order to The stimulus was presented to the right ear via insert create a composite score for correlation analyses. In light earphones (ER-3; Etymotic Research, Elk Grove Village, of auditory attention’s contribution to memory for digits IL)at80dBSPLandatarate of 4.35 Hz.Thisfastpre- forward [46], composite performance on both digits for- sentation rate limits the contribution of cortical neurons, ward and reversed subtests is referred to as Auditory which are unable to phase-lock at such fast rates [49]. Working Memory and Attention (AWM/Attn). Furthermore, the stimulus was presented in alternating polarities and average responses to each polarity were Music aptitude subsequently summed in order to limit contamination of Music aptitude was assessed using Edwin E. Gordon’s the neural recording by the cochlear microphonic [51]. Intermediate Measures of Music Audiation (IMMA) During recording sessions, participants watched videos of [47], which measures children’s abilities to internalize their choice in order to maintain a still yet wakeful state Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 4 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 Figure 1 Auditory brainstem response recording conditions. We recorded ABRs to the same speech sound in two different conditions. For the predictable condition, /da/ was repeated at a probability of 100%. In the variable condition, /da/ was randomly interspersed in the context of seven other speech sounds. We trial-matched responses to compare ABRs recorded in the variable condition to those recorded in the predictable condition without the confound of presentation order or trial event. with the soundtrack quietly playing from a speaker, audi- 10 Hz-wide bins surrounding H and H . The differences 2 4 ble through the nontest ear. Because auditory input from in the spectral amplitudes of H and H between the two 2 4 the soundtrack was not stimulus-locked and stimuli were conditions (predictable minus variable) were calculated presented directly to the right ear at a +40 dB signal-to- for each participant and normalized through conversion noise ratio, the soundtrack had no significant impact on to a z-score based on the group mean. the recorded responses [51]. Responses were digitally sampled at 20,000 Hz, offline Statistical Analyses filtered from 70 to 2000 Hz with a 12 dB roll-off and The brainstem response z-scores were compared across epoched from -40 to 190 ms (stimulus onset at time zero). conditions and groups using a Repeated Measures Events with amplitudes beyond ± 35 μV were rejected as ANOVA and correlated with the reading and music apti- artifacts. Responses to 100 μs clicks were collected before tude measures using Pearson’scorrelations(SPSS Inc., and after each recording session in order to ensure consis- Chicago, IL). RMANOVA outcomes were further defined tency of wave V latencies, confirming no differences in in apost-hocanalysisusing Mann-Whitney U-tests. All recording parameters or subject variables. results reflect two-tailed values and normality for all data As in Chandrasekaran et al. [5], we compared the brain- was confirmed using the Kolmogorov-Smirnov test for stem responses to /da/ recorded in the variable condition equality. to trial-matched responses recorded to /da/ in the predict- able condition (Figure 1). Specifically, neural responses in Structural Equation Modeling the predictable condition were averaged according to their We normalized all data through conversion to z-scores occurrence relative to the order of presentation in the vari- based on group means. Analysis of covariance matrix able condition, resulting in 700 artifact-free responses for structures was conducted with Lisrel 8.8 (Scientific Soft- each condition. ware International Inc., Lincolnwood, IL) and solutions In accordance with Chandrasekaran et al., we examined were generated based on maximum-likelihood estimation. the strength of the spectral encoding of the second and We defined the model’s directions of causality in accor- fourth harmonics (H and H ) in average responses for dance with our aims, being to define common biological 2 4 each participant over the formant transition of the stimu- and cognitive factors to account for the covariance in lus (7-60 ms in the neural response) via fast Fourier child reading and music abilities. We selected the Root transforms executed in Matlab 7.5.0 (The Mathworks, Mean Square Error of Approximation (RMSEA) in order Natick, MA). Spectral magnitudes were calculated for to evaluate the model’s goodness of fit, with measurements Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 5 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 below 0.08 indicative of good model fit [52]. Lisrel 8.8 also Music aptitude correlates with reading performance calculates the likelihood ratio (c ), its degrees of freedom Musicaptitudecorrelated with reading performance. and probability whenever maximum likelihood ratios are These relationships were largely driven by performance computed. The c test functions as a statistical method for on the Rhythm music aptitude subtest (Rhythm- evaluating structural models, describing and evaluating the TOWRE: r = 0.41, p < 0.01; Rhythm-TOSWRF: r = 0.31, p < 0.05; Tonal-TOWRE: r = 0.16, p = 0.32; Tonal- residuals that result from fitting a model to the observed TOSWRF: r = 0.26, p = 0.09), although the relationships data. A c probability value greater than 0.05 indicates a between music aptitude and reading performance were good model fit [52]. strongest when considering the composite music aptitude Results score, which considers both Tonal and Rhythm perfor- The extent of subcortical enhancement of repetitive mance (Composite-TOWRE: r = 0.45, p < 0.005; Compo- speech cues correlated with music aptitude and literacy site-TOSWRF: r = 0.39, p < 0.01). abilities. Common variance among subcortical enhance- ment of repetitive speech cues, music aptitude and read- Subcortical enhancement of predictable speech relates ing abilities was not accounted for by overarching with reading and music abilities factors such as socioeconomic status, extracurricular Poor readers showed weaker subcortical enhancement of nd th involvement or IQ. spectral components of speech sounds (2 and 4 harmo- SEM indicates that, by way of common neural (audi- nics) presented in the predictable, contrasted with the tory brainstem) and cognitive (auditory working mem- variable, condition than good readers (Figure 2a). No ory/attention) functions, music skill accounts for 38% of other significant neural differences were observed between the variance in reading performance. The resulting sta- groups, such as for the subcortical enhancement of the F tistical model delineates and quantifies relationships or other harmonics. A 2 (condition) × 2 (reading group) × among auditory brainstem function, music aptitude, 2 (harmonic) RMANOVA demonstrated an interaction memory/attention and literacy. between condition and reading group (F = 13.33, Figure 2 Subcortical enhancement of predictable speech relates with music and reading abilities. (A) Good readers demonstrate greater enhancement of speech presented in the predictable condition, compared to the variable condition, than poor readers. (B) The amount of enhancement observed in the predictable condition positively correlates with reading ability and music aptitude. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 6 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 p < 0.001). Post-hoc Mann Whitney U-tests demonstrated (r = 0.20, p = 0.20). This suggests that most of the covar- that good readers have a greater enhancement of speech iance between AWM/Attn and repetitive harmonic harmonics presented in the predictable condition than enhancement can be explained by their shared variance poor readers (H : z = -2.25, p < 0.05; H :z=-2.98,p < with music aptitude. 2 4 0.005; Figure 2a). The amount of enhancement observed in ABRs Consideration of overarching factors recorded in the predictable compared to the variable Common variance among subcortical enhancement of condition positively correlated with reading and music repetitive speech cues, music aptitude and reading abil- aptitude performance across all subjects. The reading ities could not be accounted for by overarching factors composite score (produced by combining TOWRE and such as IQ, socioeconomic status (SES) or extracurricu- TOSWRF z-scores) correlated with the amount of brain- lar involvement (ExCurr). SES and ExCurr did not cor- stem enhancement for both H and H (H :r =0.44, p relate with any of our observed variables (Table 1). IQ, 2 4 2 <0.005;H : r = 0.40, p < 0.01; Figure 2b). The music on the other hand, accounted for a significant amount composite score also correlated with the amount of of the variance in our test variables (brainstem function: brainstem enhancement to both harmonics (H :r = r = 0.37, p < 0.02; reading performance: r = 0.45, p < 0.33, p < 0.05; H : r = 0.37, p < 0.01; Figure 2b). 0.02; auditory working memory: r = 0.37, p < 0.001). Although IQ did not correlate with overall music apti- Auditory working memory and attention relate with tude or the tonal aptitude subscore (composite: r = 0.25, reading and music abilities p = 0.11; tonal: r = 0.02, p = 0.89), it correlated with the Reading and music aptitude positively correlated with rhythm aptitude subscore (r = 0.38, p < 0.02). Given performance on the auditory working memory tasks– that covarying for IQ did not eliminate the correlations memory for digits forward and digits reversed. Higher observed among our test variables (music × reading: r = AWM/Attn correlated with better reading performance 0.41, p = 0.03; music × memory/attention: r = 0.47, p = (TOWRE: r = 0.45, p < 0.005; TOSWRF: r = 0.38, p < 0.01; music × subcortical function: r = 0.41, p = 0.03; 0.01). Likewise, higher AWM/Attn correlated with reading × subcortical function: r = 0.52, p = 0.004; read- higher music aptitude (r = 0.44, p < 0.005). The rela- ing × memory/attention: r = 0.43, p = 0.04), we con- tionship between AWM/Attn and music aptitude clude that IQ did not account for the common variance appeared to be largely driven by the rhythm subtest reported among music aptitude, reading ability, working (Tonal: r = 0.203, p < 0.20; Rhythm: r = 0.49, p < 0.001; memory/attention and subcortical and cognitive Figure 3). function. Although AWM/Attn correlated with the amount of brainstem enhancement to both harmonics (r = 0.35, p < Modeling relationships among music aptitude, reading 0.05), the covariance between these measures could be ability and subcortical function accounted for by their relationships with music aptitude. In order to more comprehensively examine relationships Whereas partialing for AWM/Attn did not eliminate the among music aptitude, subcortical processing of speech common variance observed between music aptitude and regularities and reading ability, we subjected these data repetitive harmonic enhancement (r = 0.32, p = 0.04), to SEM [37]. SEM provides a mathematical method for AWM/Attn and repetitive harmonic enhancement no evaluating relationships among independent and depen- longer covaried when partialing for music aptitude dent variables in a model hypothesized apriori.Our Figure 3 Auditory working memory correlates with music aptitude. Higher rhythm, but not tonal, aptitude correlates with better auditory working memory and attention (AWM/Attn) performance. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 7 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 Table 1 Subjects’ socioeconomic status (SES) and among rhythm aptitude, subcortical enhancement of pre- extracurricular activity involvement did not correlate dictable speech harmonics and AWM/Attn in predicting with the test variables of music aptitude, auditory child reading ability. brainstem enhancement of repetitive speech cues, reading, or auditory memory/attention Discussion SES ExCurr We observed correlations among music and literacy Music aptitude -0.06, 0.72 0.02, 0.90 abilities with the extent of subcortical enhancement of Brainstem function 0.19, 0.26 0.02, 0.88 predictable speech cues. As such, our data reveal com- mon, objective neural markers for music aptitude and Reading -0.04, 0.80 0.16, 0.31 reading ability and suggest a model for the relationships Auditory memory/attention -0.01, 0.93 0.12, 0.45 that have been documented between music and literacy Table input represents Pearson’s r and p values. performance [28-31,53]. Our data also reveal common cognitive markers for hypothesized model, depicted in Figure 4, projected that music aptitude and reading ability. Auditory working music aptitude predicts reading ability by means of sub- memory and attention are driving components of child cortical processing of speech regularities and AWM/ literacy [35,36], and relationships between auditory Attn function. working memory and attention and musical skill have By means of subcortical enhancement of predictable already been established [33,54]. Not only do musicians speech harmonics and AWM, music aptitude accounted demonstrate better verbal memory than nonmusicians, for 38% of the variability in reading ability (p < 0.01). The but this advantage can be seen with as little as one year model demonstrated an excellent fit (c ( ) = 17.64, p > of musical training [55]. Our results demonstrate a simi- 0.35; RMSEA = 0.05). All path coefficients were signifi- lar relationship between auditory working memory and cant except for the path between Tonal Aptitude and attention and music aptitude in children, although this Composite Music Aptitude (r = 0.03, p = 0.31). This relationship is observed regardless of musical training model emphasizes the combined strength of relationships backgrounds. Figure 4 Structural equation model (SEM) of music aptitude, reading, auditory working memory/attention and auditory brainstem function. Music aptitude accounts for 38% of the variability in reading ability through its impact on auditory working memory/attention and subcortical enhancement of predictable speech harmonics. The model demonstrates an excellent fit; values plotted represent squared correlation coefficients (r ). *p < 0.05; **p < 0.01; ***p < 0.001. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 8 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 The role of the descending auditory system It is not surprising that we observed correlations As in Chandrasekaran et al., we observed subcortical between music aptitude and subcortical spectral enhance- enhancement of a predictable, contrasted with a variable, ment of predictable speech sounds given that musical speech presentation [5]. This enhancement was specific expertise increases one’s sensitivity to sound patterns not for frequencies integral to the perception of pitch (H only in music, but also in speech [34,69]. Although the and H ). Similar repetition-induced frequency enhance- argument can be made for a genetic contributor to musi- ment has been observed in the primary auditory cortex, cians’ enhanced sound processing, this increased sensitiv- where neurons exhibit sharpened acuity to stimulus fre- ity can be modulated, at least in part, by one’smethodof quency [16]. This tuning occurs without overt attention, musical practice and training [70]. Furthermore, diverse is stimulus specific and develops rapidly [3,56]. Not sur- methodological approaches consistently reveal correlations prisingly, enhanced neural tuning with stimulus repeti- between the extent of structural and functional neural tion has been proposed to relate with improved object enhancement observed in musicians and their years of discrimination [16,18]. musical practice or age of practice onset [71-74]. Such The ability of the sensory system to automatically mod- observations suggest the substantial contribution of ify neural response properties according to expectations experience-induced neuroplasticity to musicians’ enhanced in a dynamic and context-sensitive manner is thought to sound processing and may be attributed to the strength of have evolved to infer and represent the causes of change top-down contributors to auditory processing [33,69]. in our environment [1,57]. This modification may occur in a descending fashion, beginning in extra-sensory cor- Subcortical enhancement of predictable speech: tices where predictions are developed based on prior implications for reading impairment experience (such as with repetition) and sequentially tun- Due to its multisensory nature, attentional demands and ing lower level response properties to heighten sensory reliance on rapid audio-motor feedback, music is a acuity [2,32,57,58]. The descending nature of this neural powerful tool for engendering neural plasticity, particu- tuning is supported by observations from cortical work larly for auditory processing [34,75-78]. This plasticity is showing decreased onset latencies from 120 ms (after not constrained to the brain’s music networks but applies two repetitions) to 50 ms (after 30 repetitions) [56] and is more generally to auditory functions [27,69,72,79-82]. thought to represent the strengthening of the stimulus- Clinicians and researchers involved in the treatment and specific memory trace at earlier and earlier processing assessment of reading dysfunction have long held interest stages [3]. The correlations reported here between music in the potential for musical training to strengthen neural aptitude and reading ability with subcortical fine-tuning networks for reading. Wisbey was one of the first to for- to predictable speech sounds may indicate stronger top- mally propose that music, by facilitating the development down modulatory systems in individuals with better of multisensory awareness and auditory acuity, could music aptitude and reading performance. promote reading in impaired children [83]. This proposal has been verified by a number of experiments [84,85] (c.f. Musical experience boosts sensitivity to sound patterns Morais et al., 2010 [25]), with relationships between Our data demonstrate that diminished subcortical music and reading abilities observed in many more enhancement of predictable speech sounds relates with [28-30,53,86]. reading impairment. Similar observations have been Definition and characterization of common neural made in poor readers, in addition to children with poor mechanisms for music and reading skills may enable perception of speech presented in background noise [5]; the development of a biological assessment of reading we extend these findings to the domain of music. This impairment and improve the efficacy of remedial attempts. relationship is not surprising given the importance of Reading performance is known to rely on a chorus of mul- sound repetition and sequencing for music perception. tifaceted and complex processes that have proven difficult Specifically, repetition and regularity lends to the percep- to disentangle; here, we find that subcortical function tion of tonality [59], rhythm and meter [60,61] and the serves as a significant and accessible factor in reading structural use of musical themes. Deviations from pre- impairment, accounting for 44% of the variance in child dicted patterns result in impaired music production and reading ability. The use of auditory brainstem measure- perception [62-64] and can be flagged by the auditory ments to assess learning and reading impairment has cortex in both musically trained and untrained indivi- emerged in recent years [21,87,88], is being adapted for duals, as measured by auditory evoked potentials [65-67]. theclinicand canprovideanobjectiveindex of thesuc- Increased sensitivity to deviations from patterns in musi- cess of auditory [89,90] and music training [21]. In light of cal sound is thought to reflect enhanced sensory memory the high test-retest reliability of the speech-evoked ABR and discrimination abilities as well as more firmly estab- [91], individual responses are highly replicable and can be lished categorical boundaries [68]. meaningfully compared to group means or established Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 9 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 norms. Identification of common neural markers for ability. Further outcomes reveal direct relationships music and reading skill, such as those reported here, may between musical skill and literacy-related aspects of audi- lead to the biological assessment of music-associated tory brainstem and memory/attention function, revealing learning abilities in children and encourage the employ- common neural and cognitive mechanisms for reading ment of music as a technique for literacy remediation. and music abilities that may operate, at least in part, via Musical training during early childhood may be parti- corticofugal shaping of sensory function. By way of audi- cularly important for the advancement of music and tory brainstem spectral enhancement of predictable reading aptitude. Although the music test employed here speech and auditory working memory/attention, music is thought to measure music aptitude, being one’s inher- skill predicts approximately 40% of the variance in read- ent ability for music, the creator of this measure, Edwin ing performance. Definition of common neural and cog- E. Gordon, has long emphasized the impact of music nitive mechanisms for music and reading skills may education during early childhood on music aptitude support the usefulness of music for promoting child lit- scores. Gordon makes this claim in light of his extensive eracy, with the potential to improve the efficacy of reme- longitudinal work showing that music aptitude can dial attempts. improve with musical training, particularly during early childhood [92]. The importance of an early onset of Appendix A music activities is more directly supported by outcomes Grouping according to good and poor music aptitude from neuroscientific research, in which many of the neu- The extent of brainstem enhancement of predictable th roplastic changes associated with musical training are speech in subjects with high (IMMA ≥70 percentile; n = th more extensive in individuals who began training earlier 18) and low (IMMA ≤30 percentile; n = 9) music apti- in their lifetimes [71,72,93-96]. With regard to auditory tude patterned with the results observed when subjects brainstem processing, we found that ABRs in young were divided into good and poor readers. A 2 (condition) adult musicians who began musical training prior to age × 2 (music group) × 2 (harmonic) RMANOVA demon- 7 were distinct from those in musicians who began train- strated an interaction between condition and music ing between the ages of 7-13 [72,93]. Whereas musicians group (F = 6.17, p < 0.02). Post-hoc Mann Whitney U- who began training prior to age 7 demonstrated tests demonstrated that subjects with high music aptitude enhanced ABRs to the spectral components of communi- have a greater enhancement of the second harmonic of cation sounds compared to nonmusicians, those who speech presented in the predictable condition compared began later in life did not. Observations such as this to the variable condition than subjects with low music reflect a critical period for musical training-associated aptitude (H : z = -1.96, p < 0.05; H : z = -1.29, p = 0.19). 2 4 neural plasticity [97] and may speak to the importance of initiating musical training during early childhood for Acknowledgements bringing about the greatest impact on music aptitude or, This work is supported by the National Science Foundation grant 0921275 we propose, reading ability. to NK and the National Institutes of Health grant F31DC011457 to DS. It remains undetermined whether reading abilities are Author details impacted alongside music aptitude with musical training 1 Auditory Neuroscience Laboratory, Northwestern University, Evanston, IL, during childhood or whether the neural mechanism USA. Institute for Neuroscience, Northwestern University, Chicago, IL, USA. Department of Communication Sciences, Northwestern University, Evanston, reported here is affected by musical training. Also undeter- IL, USA. Department of Neurobiology and Physiology, Northwestern mined is whether relationships between music and reading 5 University, Evanston, IL, USA. Department of Otolaryngology, Northwestern work in reverse, with language-based literacy remediation University, Chicago, IL, USA. leading to improved music aptitude. More work (notably, Authors’ contributions longitudinal work) is necessary in order to define relation- DS collected the data, conducted and interpreted the statistical analyses and ships between music aptitude, literacy and the auditory prepared the manuscript. JH collected and processed the data, provided consultation with respect to statistical methods and reviewed the drafts of brainstem response to speech as well as to determine the the manuscript. NK oversaw all aspects of the study and reviewed the drafts impact of formal training, the efficacy of specific training of the manuscript. All authors read and approved the final manuscript. approaches and/or literacy remediation programs. Competing interests The authors declare that they have no competing interests. Conclusions Reading relies on a complex and multifaceted combina- Received: 12 May 2011 Accepted: 17 October 2011 Published: 17 October 2011 tion of processes that have proven difficult to disentangle. 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J Res Reading 1994, 17:99-107. 85. Moreno S, Marques C, Santos A, Santos M, Castro SL, Besson M: Musical training influences linguistic abilities in 8-year-old children: More evidence for brain plasticity. Cereb Cortex 2009, 19:712-23. Submit your next manuscript to BioMed Central 86. Overy K, Nicolson RI, Fawcett AJ, Clarke EF: Dyslexia and music: Measuring and take full advantage of: musical timing skills. Dyslexia 2003, 9:18-36. 87. Banai K, Hornickel J, Skoe E, Nicol T, Zecker S, Kraus N: Reading and • Convenient online submission subcortical auditory function. Cereb Cortex 2009, 19:2699-707. 88. Hornickel J, Skoe E, Nicol T, Zecker S, Kraus N: Subcortical differentiation of • Thorough peer review voiced stop consonants: Relationships to reading and speech in noise • No space constraints or color figure charges perception. Proc Natl Acad Sci USA 2009, 106:13022-13027. • Immediate publication on acceptance 89. Russo NM, Nicol TG, Zecker SG, Hayes EA, Kraus N: Auditory training improves neural timing in the human brainstem. Behav Brain Res 2005, • Inclusion in PubMed, CAS, Scopus and Google Scholar 156:95-103. • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral and Brain Functions Springer Journals

Subcortical processing of speech regularities underlies reading and music aptitude in children

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Springer Journals
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Copyright © 2011 by Strait et al; licensee BioMed Central Ltd.
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Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
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Abstract

Background: Neural sensitivity to acoustic regularities supports fundamental human behaviors such as hearing in noise and reading. Although the failure to encode acoustic regularities in ongoing speech has been associated with language and literacy deficits, how auditory expertise, such as the expertise that is associated with musical skill, relates to the brainstem processing of speech regularities is unknown. An association between musical skill and neural sensitivity to acoustic regularities would not be surprising given the importance of repetition and regularity in music. Here, we aimed to define relationships between the subcortical processing of speech regularities, music aptitude, and reading abilities in children with and without reading impairment. We hypothesized that, in combination with auditory cognitive abilities, neural sensitivity to regularities in ongoing speech provides a common biological mechanism underlying the development of music and reading abilities. Methods: We assessed auditory working memory and attention, music aptitude, reading ability, and neural sensitivity to acoustic regularities in 42 school-aged children with a wide range of reading ability. Neural sensitivity to acoustic regularities was assessed by recording brainstem responses to the same speech sound presented in predictable and variable speech streams. Results: Through correlation analyses and structural equation modeling, we reveal that music aptitude and literacy both relate to the extent of subcortical adaptation to regularities in ongoing speech as well as with auditory working memory and attention. Relationships between music and speech processing are specifically driven by performance on a musical rhythm task, underscoring the importance of rhythmic regularity for both language and music. Conclusions: These data indicate common brain mechanisms underlying reading and music abilities that relate to how the nervous system responds to regularities in auditory input. Definition of common biological underpinnings for music and reading supports the usefulness of music for promoting child literacy, with the potential to improve reading remediation. The human nervous system makes use of sensory regula- regularly-occurring, as opposed to unpredictably-occur- rities to drive accurate perception, especially when con- ring, stimuli [3-5]. The brain’s ability to use sensory regu- fronted with challenging perceptual environments [1]. It larities is a fundamental feature of auditory processing, is thought that the brain shapes perception according to promoting even the most basic of auditory experiences predictions that are made based on regularities; this such as language processing during infancy [6,7] and shaping is accomplished by comparing higher-level pre- speech comprehension amidst a competing conversa- tional background [5]. Failure of the brain to utilize dictions with lower-level sensory encoding of an incom- ing stimulus via the corticofugal (i.e., top down) system sensory regularities has been associated with neural dys- [2]. This is a common neural feature that spans sensory function, such as schizophrenia [8] and language impair- modalities and can be observed in neural responses to ment (e.g., dyslexia) [5,9-11]. The impact of stimulus regularity on auditory proces- sing has been well established in the auditory cortex [1,3] * Correspondence: nkraus@northwestern.edu Auditory Neuroscience Laboratory, Northwestern University, Evanston, IL, and was recently documented at and below the level of USA the brainstem [12-15]. Specifically, neural potentials to Full list of author information is available at the end of the article © 2011 Strait et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 2 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 frequently-occurring sounds exhibit enhanced frequency biological underpinnings for music and reading abilities. tuning in both the primary auditory cortex [16] and in We anticipated that music aptitude and literacy abilities the auditory brainstem [5,17]. This sensory fine-tuning would positively correlate with subcortical spectral occurs rapidly, does not require overt attention and may enhancement of repetitive speech cues. We also explored enable enhanced object discrimination [14,18]. Although relationships between musical skill and literacy-related reference to the neural enhancement of a repeated aspects of auditory cognitive function through working memory assessments [35,36], which included an auditory speech sound might seem contradictory to the well- attention component. We anticipated that music aptitude known repetition suppression of cortical evoked response and literacy abilities would positively correlate with audi- magnitudes, the neural mechanisms underlying this effect remain debated. While some have proposed that stimulus tory working memory and attention performance. In repetition leads to overall decreased neuronal activity, order to delineate and quantify relationships among vari- others have suggested that repetition facilitates precision ables, we applied the data to Structural Equation Model- in neural representation by enhancing certain aspects of ing (SEM). SEM relies on a variety of simultaneous the neural response while inhibiting others (e.g., more statistical methods (e.g., factor analysis, multiple regres- precise inhibitory sidebands surrounding a facilitated sions and path analysis combined with structural equa- response to the physical dimensions of a repeated stimu- tion relations) to evaluate a hypothesized model [37]. lus) [4]. Although more traditional regression analyses are useful Human auditory brainstem responses (ABRs) to the for delineating causal relationships among variables, SEM pitch of predictably presented speech are enhanced rela- enables more efficient characterization of complex, real- tive to ABRs to speech presented in a variable context world processes than can be achieved using correlation- [5]. The extent of this subcortical enhancement of regu- based analyses [38]. Specific benefits of SEM include the larly-occurring speech relates to better performance on simultaneous analysis of multiple interrelated variables, language-related tasks, such as reading and hearing consideration of measurement error, and inherent con- speech in noise. This fine-tuning is thought to be driven trol for multiple comparisons. We expected SEM to sub- by top-down cortical modulation of subcortical response stantiate our hypothesis that music aptitude predicts properties [19] and its absence in poor readers is consis- much of the variance in literacy abilities by way of shared tent with proposals that child reading impairment stems cognitive and neural mechanisms. from the brain’s inability to benefit from repetition in the sensory stream. Specifically, children with dyslexia fail to Materials and methods form perceptual anchors–a type of perceptual memory– Participants based on repeating sounds [9,11]. 42 normal hearing children between the ages of 8-13 Although we have made gains in understanding the years (M = 10.4, SD = 1.6, Males = 26). Participants and auditory processing of speech regularities in children their legal guardians provided informed assent and con- with reading impairment (or lack thereof), we do not sent according to Northwestern University’s Institutional know how auditory expertise shapes these mechanisms. Review Board. Because we aimed to evaluate neural func- The auditory expertise engendered by musical training tion and music aptitude across a spectrum of readers, no during childhood and into adulthood promotes the sub- literacy restrictions were applied but all participants cortical encoding of speech [20,21] and may strengthen demonstrated normal audiometric thresholds (≤20 dB neural mechanisms that undergird child literacy [22-24]. HL pure tone thresholds at octave frequencies from 125 Although the integrative nature of music and language to 8000 Hz) and IQ (≥85 score on the Wechsler Abbre- abilities continues to be debated [25-27], a growing body viated Scale of Intelligence) [39]. Participants also had of work supports shared abilities for music and reading, clinically normal ABRs to 80 dB SPL 100 μs click stimuli with music aptitude accounting for a substantial amount that were presented at 31.1 Hz. of the variance in child reading ability [28-30] even after Extent of extracurricular activity was assessed by a par- controlling for nonverbal IQ and phonological awareness ent questionnaire (the Child Behavior Checklist [40]). Par- [31]. It is thought that strengthened top-down control, ents rated their child’s current extracurricular activities which is important for modulating lower-level neural according to the frequency of the child’s involvement–less responses, unfolds with expertise [32] and, more specifi- than average, average, or more than average; these scores cally, with musical training [33,34]. were summed to produce a single extracurricular activity In order to define relationships between musical skill score. and literacy-related aspects of auditory brainstem func- Good (n = 8) and poor readers (n = 21) were differen- tion, we assessed subcortical processing of speech regula- tiated based on reading ability (Test of Word Reading rities, music aptitude and reading abilities in school-aged Efficiency; see Reading and working memory,below) [5]. children. Our overarching goal was to define common Children with scores ≤90 were included in the poor Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 3 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 reading group, while good readers had scores ≥110. 13 musical sound and compare two sequentially presented subjects did not meet the criteria for either group and sound patterns. Tonal aptitude was assessed by the were excluded from group analyses. Good and poor read- Tonal subtest, in which participants are presented with ers did not differ in age (Mann-Whitney U test; z = 40 pairs of musical excerpts that do not differ rhythmi- -0.223, p = 0.83), sex (Pearson Chi-Square c =0.12, p= cally but may differ melodically. Rhythm aptitude was 0.73), socioeconomic status as inferred by maternal edu- assessed by the Rhythm subtest, in which participants cation [41] (Pearson Chi-Square c = 1.10, p = 0.59), are presented with 40 pairs of short excerpts that do years of musical training (Mann-Whitney U test; z = not differ melodically but may differ rhythmically. For -0.231, p = 0.82), extent of extracurricular activity both subtests, participants indicate whether the two (Mann-Whitney U test; z = -1.202, p = 0.23) or nonverbal excerpts in each pair are the same or different. The IQ (Mann-Whitney U test; z = -1.834, p = 0.07). With subtest scores are combined to generate a composite regard to musical training histories, 36 of the 42 children music aptitude score. The rhythm, tonal and composite had undergone no to only a few months of musical train- scores are normed by academic grade in order to pro- ing and were not currently involved in music activities. duce percentile rankings. The other six children had participated in at least one year of musical training. One of these children was cate- Auditory brainstem measures gorized as a poor reader, two were categorized as good Brainstem responses to the speech sound /da/ were col- readers and three were considered average readers (as lected from Cz using Scan 4.3 (Compumedics, Charlotte, such, these three were not included in either reading NC) under two conditions. Ag-AgCl electrodes were group). applied in a vertical, ipsilateral montage (i.e., FPz as ground, right earlobe as reference). Evoked potentials Reading and working memory recorded with this electrode montage have been found to Standardized literacy measures assessed oral (Test of reflect activity from an ensemble of neural elements of Word Reading Efficiency, TOWRE) [42] and silent (Test central brainstem origin [48,49]. In the predictable condi- of Silent Word Reading Fluency, TOSWRF) [43] reading tion, the speech sound /da/ was presented at a probability speed. The TOWRE requires children to read aloud lists of 100%, whereas in the variable condition /da/ was ran- of real words (Sight subtest) and nonsense words (Phone- domly interspersed in the context of seven other speech mic Decoding subtest) while being timed. The two sub- sounds at a probability of 13% (Figure 1). The seven scores are combined to form a composite score (here speech sounds varied acoustically according to a variety referred to as the TOWRE). The TOSWRF requires parti- of features, including formant structure (/ba/, /ga/, /du/), cipants to quickly identify printed words by demarcating duration (a 163 ms /da/), voice-onset-time (/ta/) and F lines of letters into individual words while being timed. (250 Hz /da/, /da/ with a dipping pitch contour). The Participants are presented with rows of words that gradu- /da/ stimulus was a six-formant, 170 ms speech syllable ally increase in reading difficulty and they are asked to synthesized in Klatt [50] with a 5 ms voice onset time separate them (e.g., dimhowfigblue ® dim/how/fig/blue). and a level fundamental frequency (F , 100 Hz). The first, TOWRE ("reading efficiency”) and TOSWRF ("reading flu- second and third formants were dynamic over the first 50 ency”) age-normed scores were averaged in order to create ms (F , 400-720 Hz; F , 1700-1240 Hz; F , 2580-2500 Hz) 1 2 3 a composite Reading variable for correlation analyses. and then maintained frequency for the rest of the dura- Auditory working memory was assessed using the tion. The fourth, fifth and sixth formants were constant Memory for Digits Forward subtest of the Comprehen- throughout the entire duration of the stimulus (F , 3300 sive Test of Phonological Processing [44] and the Mem- Hz; F ,3750Hz; F , 4900 Hz). For a detailed description 5 6 ory for Digits Reversed subtest of the Woodcock Johnson of the seven other speech sounds, see Chandrasekaran Test of Cognitive Abilities [45]. Digits forward and digits et al. (2009). reversed age-normed scores were averaged in order to The stimulus was presented to the right ear via insert create a composite score for correlation analyses. In light earphones (ER-3; Etymotic Research, Elk Grove Village, of auditory attention’s contribution to memory for digits IL)at80dBSPLandatarate of 4.35 Hz.Thisfastpre- forward [46], composite performance on both digits for- sentation rate limits the contribution of cortical neurons, ward and reversed subtests is referred to as Auditory which are unable to phase-lock at such fast rates [49]. Working Memory and Attention (AWM/Attn). Furthermore, the stimulus was presented in alternating polarities and average responses to each polarity were Music aptitude subsequently summed in order to limit contamination of Music aptitude was assessed using Edwin E. Gordon’s the neural recording by the cochlear microphonic [51]. Intermediate Measures of Music Audiation (IMMA) During recording sessions, participants watched videos of [47], which measures children’s abilities to internalize their choice in order to maintain a still yet wakeful state Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 4 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 Figure 1 Auditory brainstem response recording conditions. We recorded ABRs to the same speech sound in two different conditions. For the predictable condition, /da/ was repeated at a probability of 100%. In the variable condition, /da/ was randomly interspersed in the context of seven other speech sounds. We trial-matched responses to compare ABRs recorded in the variable condition to those recorded in the predictable condition without the confound of presentation order or trial event. with the soundtrack quietly playing from a speaker, audi- 10 Hz-wide bins surrounding H and H . The differences 2 4 ble through the nontest ear. Because auditory input from in the spectral amplitudes of H and H between the two 2 4 the soundtrack was not stimulus-locked and stimuli were conditions (predictable minus variable) were calculated presented directly to the right ear at a +40 dB signal-to- for each participant and normalized through conversion noise ratio, the soundtrack had no significant impact on to a z-score based on the group mean. the recorded responses [51]. Responses were digitally sampled at 20,000 Hz, offline Statistical Analyses filtered from 70 to 2000 Hz with a 12 dB roll-off and The brainstem response z-scores were compared across epoched from -40 to 190 ms (stimulus onset at time zero). conditions and groups using a Repeated Measures Events with amplitudes beyond ± 35 μV were rejected as ANOVA and correlated with the reading and music apti- artifacts. Responses to 100 μs clicks were collected before tude measures using Pearson’scorrelations(SPSS Inc., and after each recording session in order to ensure consis- Chicago, IL). RMANOVA outcomes were further defined tency of wave V latencies, confirming no differences in in apost-hocanalysisusing Mann-Whitney U-tests. All recording parameters or subject variables. results reflect two-tailed values and normality for all data As in Chandrasekaran et al. [5], we compared the brain- was confirmed using the Kolmogorov-Smirnov test for stem responses to /da/ recorded in the variable condition equality. to trial-matched responses recorded to /da/ in the predict- able condition (Figure 1). Specifically, neural responses in Structural Equation Modeling the predictable condition were averaged according to their We normalized all data through conversion to z-scores occurrence relative to the order of presentation in the vari- based on group means. Analysis of covariance matrix able condition, resulting in 700 artifact-free responses for structures was conducted with Lisrel 8.8 (Scientific Soft- each condition. ware International Inc., Lincolnwood, IL) and solutions In accordance with Chandrasekaran et al., we examined were generated based on maximum-likelihood estimation. the strength of the spectral encoding of the second and We defined the model’s directions of causality in accor- fourth harmonics (H and H ) in average responses for dance with our aims, being to define common biological 2 4 each participant over the formant transition of the stimu- and cognitive factors to account for the covariance in lus (7-60 ms in the neural response) via fast Fourier child reading and music abilities. We selected the Root transforms executed in Matlab 7.5.0 (The Mathworks, Mean Square Error of Approximation (RMSEA) in order Natick, MA). Spectral magnitudes were calculated for to evaluate the model’s goodness of fit, with measurements Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 5 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 below 0.08 indicative of good model fit [52]. Lisrel 8.8 also Music aptitude correlates with reading performance calculates the likelihood ratio (c ), its degrees of freedom Musicaptitudecorrelated with reading performance. and probability whenever maximum likelihood ratios are These relationships were largely driven by performance computed. The c test functions as a statistical method for on the Rhythm music aptitude subtest (Rhythm- evaluating structural models, describing and evaluating the TOWRE: r = 0.41, p < 0.01; Rhythm-TOSWRF: r = 0.31, p < 0.05; Tonal-TOWRE: r = 0.16, p = 0.32; Tonal- residuals that result from fitting a model to the observed TOSWRF: r = 0.26, p = 0.09), although the relationships data. A c probability value greater than 0.05 indicates a between music aptitude and reading performance were good model fit [52]. strongest when considering the composite music aptitude Results score, which considers both Tonal and Rhythm perfor- The extent of subcortical enhancement of repetitive mance (Composite-TOWRE: r = 0.45, p < 0.005; Compo- speech cues correlated with music aptitude and literacy site-TOSWRF: r = 0.39, p < 0.01). abilities. Common variance among subcortical enhance- ment of repetitive speech cues, music aptitude and read- Subcortical enhancement of predictable speech relates ing abilities was not accounted for by overarching with reading and music abilities factors such as socioeconomic status, extracurricular Poor readers showed weaker subcortical enhancement of nd th involvement or IQ. spectral components of speech sounds (2 and 4 harmo- SEM indicates that, by way of common neural (audi- nics) presented in the predictable, contrasted with the tory brainstem) and cognitive (auditory working mem- variable, condition than good readers (Figure 2a). No ory/attention) functions, music skill accounts for 38% of other significant neural differences were observed between the variance in reading performance. The resulting sta- groups, such as for the subcortical enhancement of the F tistical model delineates and quantifies relationships or other harmonics. A 2 (condition) × 2 (reading group) × among auditory brainstem function, music aptitude, 2 (harmonic) RMANOVA demonstrated an interaction memory/attention and literacy. between condition and reading group (F = 13.33, Figure 2 Subcortical enhancement of predictable speech relates with music and reading abilities. (A) Good readers demonstrate greater enhancement of speech presented in the predictable condition, compared to the variable condition, than poor readers. (B) The amount of enhancement observed in the predictable condition positively correlates with reading ability and music aptitude. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 6 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 p < 0.001). Post-hoc Mann Whitney U-tests demonstrated (r = 0.20, p = 0.20). This suggests that most of the covar- that good readers have a greater enhancement of speech iance between AWM/Attn and repetitive harmonic harmonics presented in the predictable condition than enhancement can be explained by their shared variance poor readers (H : z = -2.25, p < 0.05; H :z=-2.98,p < with music aptitude. 2 4 0.005; Figure 2a). The amount of enhancement observed in ABRs Consideration of overarching factors recorded in the predictable compared to the variable Common variance among subcortical enhancement of condition positively correlated with reading and music repetitive speech cues, music aptitude and reading abil- aptitude performance across all subjects. The reading ities could not be accounted for by overarching factors composite score (produced by combining TOWRE and such as IQ, socioeconomic status (SES) or extracurricu- TOSWRF z-scores) correlated with the amount of brain- lar involvement (ExCurr). SES and ExCurr did not cor- stem enhancement for both H and H (H :r =0.44, p relate with any of our observed variables (Table 1). IQ, 2 4 2 <0.005;H : r = 0.40, p < 0.01; Figure 2b). The music on the other hand, accounted for a significant amount composite score also correlated with the amount of of the variance in our test variables (brainstem function: brainstem enhancement to both harmonics (H :r = r = 0.37, p < 0.02; reading performance: r = 0.45, p < 0.33, p < 0.05; H : r = 0.37, p < 0.01; Figure 2b). 0.02; auditory working memory: r = 0.37, p < 0.001). Although IQ did not correlate with overall music apti- Auditory working memory and attention relate with tude or the tonal aptitude subscore (composite: r = 0.25, reading and music abilities p = 0.11; tonal: r = 0.02, p = 0.89), it correlated with the Reading and music aptitude positively correlated with rhythm aptitude subscore (r = 0.38, p < 0.02). Given performance on the auditory working memory tasks– that covarying for IQ did not eliminate the correlations memory for digits forward and digits reversed. Higher observed among our test variables (music × reading: r = AWM/Attn correlated with better reading performance 0.41, p = 0.03; music × memory/attention: r = 0.47, p = (TOWRE: r = 0.45, p < 0.005; TOSWRF: r = 0.38, p < 0.01; music × subcortical function: r = 0.41, p = 0.03; 0.01). Likewise, higher AWM/Attn correlated with reading × subcortical function: r = 0.52, p = 0.004; read- higher music aptitude (r = 0.44, p < 0.005). The rela- ing × memory/attention: r = 0.43, p = 0.04), we con- tionship between AWM/Attn and music aptitude clude that IQ did not account for the common variance appeared to be largely driven by the rhythm subtest reported among music aptitude, reading ability, working (Tonal: r = 0.203, p < 0.20; Rhythm: r = 0.49, p < 0.001; memory/attention and subcortical and cognitive Figure 3). function. Although AWM/Attn correlated with the amount of brainstem enhancement to both harmonics (r = 0.35, p < Modeling relationships among music aptitude, reading 0.05), the covariance between these measures could be ability and subcortical function accounted for by their relationships with music aptitude. In order to more comprehensively examine relationships Whereas partialing for AWM/Attn did not eliminate the among music aptitude, subcortical processing of speech common variance observed between music aptitude and regularities and reading ability, we subjected these data repetitive harmonic enhancement (r = 0.32, p = 0.04), to SEM [37]. SEM provides a mathematical method for AWM/Attn and repetitive harmonic enhancement no evaluating relationships among independent and depen- longer covaried when partialing for music aptitude dent variables in a model hypothesized apriori.Our Figure 3 Auditory working memory correlates with music aptitude. Higher rhythm, but not tonal, aptitude correlates with better auditory working memory and attention (AWM/Attn) performance. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 7 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 Table 1 Subjects’ socioeconomic status (SES) and among rhythm aptitude, subcortical enhancement of pre- extracurricular activity involvement did not correlate dictable speech harmonics and AWM/Attn in predicting with the test variables of music aptitude, auditory child reading ability. brainstem enhancement of repetitive speech cues, reading, or auditory memory/attention Discussion SES ExCurr We observed correlations among music and literacy Music aptitude -0.06, 0.72 0.02, 0.90 abilities with the extent of subcortical enhancement of Brainstem function 0.19, 0.26 0.02, 0.88 predictable speech cues. As such, our data reveal com- mon, objective neural markers for music aptitude and Reading -0.04, 0.80 0.16, 0.31 reading ability and suggest a model for the relationships Auditory memory/attention -0.01, 0.93 0.12, 0.45 that have been documented between music and literacy Table input represents Pearson’s r and p values. performance [28-31,53]. Our data also reveal common cognitive markers for hypothesized model, depicted in Figure 4, projected that music aptitude and reading ability. Auditory working music aptitude predicts reading ability by means of sub- memory and attention are driving components of child cortical processing of speech regularities and AWM/ literacy [35,36], and relationships between auditory Attn function. working memory and attention and musical skill have By means of subcortical enhancement of predictable already been established [33,54]. Not only do musicians speech harmonics and AWM, music aptitude accounted demonstrate better verbal memory than nonmusicians, for 38% of the variability in reading ability (p < 0.01). The but this advantage can be seen with as little as one year model demonstrated an excellent fit (c ( ) = 17.64, p > of musical training [55]. Our results demonstrate a simi- 0.35; RMSEA = 0.05). All path coefficients were signifi- lar relationship between auditory working memory and cant except for the path between Tonal Aptitude and attention and music aptitude in children, although this Composite Music Aptitude (r = 0.03, p = 0.31). This relationship is observed regardless of musical training model emphasizes the combined strength of relationships backgrounds. Figure 4 Structural equation model (SEM) of music aptitude, reading, auditory working memory/attention and auditory brainstem function. Music aptitude accounts for 38% of the variability in reading ability through its impact on auditory working memory/attention and subcortical enhancement of predictable speech harmonics. The model demonstrates an excellent fit; values plotted represent squared correlation coefficients (r ). *p < 0.05; **p < 0.01; ***p < 0.001. Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 8 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 The role of the descending auditory system It is not surprising that we observed correlations As in Chandrasekaran et al., we observed subcortical between music aptitude and subcortical spectral enhance- enhancement of a predictable, contrasted with a variable, ment of predictable speech sounds given that musical speech presentation [5]. This enhancement was specific expertise increases one’s sensitivity to sound patterns not for frequencies integral to the perception of pitch (H only in music, but also in speech [34,69]. Although the and H ). Similar repetition-induced frequency enhance- argument can be made for a genetic contributor to musi- ment has been observed in the primary auditory cortex, cians’ enhanced sound processing, this increased sensitiv- where neurons exhibit sharpened acuity to stimulus fre- ity can be modulated, at least in part, by one’smethodof quency [16]. This tuning occurs without overt attention, musical practice and training [70]. Furthermore, diverse is stimulus specific and develops rapidly [3,56]. Not sur- methodological approaches consistently reveal correlations prisingly, enhanced neural tuning with stimulus repeti- between the extent of structural and functional neural tion has been proposed to relate with improved object enhancement observed in musicians and their years of discrimination [16,18]. musical practice or age of practice onset [71-74]. Such The ability of the sensory system to automatically mod- observations suggest the substantial contribution of ify neural response properties according to expectations experience-induced neuroplasticity to musicians’ enhanced in a dynamic and context-sensitive manner is thought to sound processing and may be attributed to the strength of have evolved to infer and represent the causes of change top-down contributors to auditory processing [33,69]. in our environment [1,57]. This modification may occur in a descending fashion, beginning in extra-sensory cor- Subcortical enhancement of predictable speech: tices where predictions are developed based on prior implications for reading impairment experience (such as with repetition) and sequentially tun- Due to its multisensory nature, attentional demands and ing lower level response properties to heighten sensory reliance on rapid audio-motor feedback, music is a acuity [2,32,57,58]. The descending nature of this neural powerful tool for engendering neural plasticity, particu- tuning is supported by observations from cortical work larly for auditory processing [34,75-78]. This plasticity is showing decreased onset latencies from 120 ms (after not constrained to the brain’s music networks but applies two repetitions) to 50 ms (after 30 repetitions) [56] and is more generally to auditory functions [27,69,72,79-82]. thought to represent the strengthening of the stimulus- Clinicians and researchers involved in the treatment and specific memory trace at earlier and earlier processing assessment of reading dysfunction have long held interest stages [3]. The correlations reported here between music in the potential for musical training to strengthen neural aptitude and reading ability with subcortical fine-tuning networks for reading. Wisbey was one of the first to for- to predictable speech sounds may indicate stronger top- mally propose that music, by facilitating the development down modulatory systems in individuals with better of multisensory awareness and auditory acuity, could music aptitude and reading performance. promote reading in impaired children [83]. This proposal has been verified by a number of experiments [84,85] (c.f. Musical experience boosts sensitivity to sound patterns Morais et al., 2010 [25]), with relationships between Our data demonstrate that diminished subcortical music and reading abilities observed in many more enhancement of predictable speech sounds relates with [28-30,53,86]. reading impairment. Similar observations have been Definition and characterization of common neural made in poor readers, in addition to children with poor mechanisms for music and reading skills may enable perception of speech presented in background noise [5]; the development of a biological assessment of reading we extend these findings to the domain of music. This impairment and improve the efficacy of remedial attempts. relationship is not surprising given the importance of Reading performance is known to rely on a chorus of mul- sound repetition and sequencing for music perception. tifaceted and complex processes that have proven difficult Specifically, repetition and regularity lends to the percep- to disentangle; here, we find that subcortical function tion of tonality [59], rhythm and meter [60,61] and the serves as a significant and accessible factor in reading structural use of musical themes. Deviations from pre- impairment, accounting for 44% of the variance in child dicted patterns result in impaired music production and reading ability. The use of auditory brainstem measure- perception [62-64] and can be flagged by the auditory ments to assess learning and reading impairment has cortex in both musically trained and untrained indivi- emerged in recent years [21,87,88], is being adapted for duals, as measured by auditory evoked potentials [65-67]. theclinicand canprovideanobjectiveindex of thesuc- Increased sensitivity to deviations from patterns in musi- cess of auditory [89,90] and music training [21]. In light of cal sound is thought to reflect enhanced sensory memory the high test-retest reliability of the speech-evoked ABR and discrimination abilities as well as more firmly estab- [91], individual responses are highly replicable and can be lished categorical boundaries [68]. meaningfully compared to group means or established Strait et al. Behavioral and Brain Functions 2011, 7:44 Page 9 of 11 http://www.behavioralandbrainfunctions.com/content/7/1/44 norms. Identification of common neural markers for ability. Further outcomes reveal direct relationships music and reading skill, such as those reported here, may between musical skill and literacy-related aspects of audi- lead to the biological assessment of music-associated tory brainstem and memory/attention function, revealing learning abilities in children and encourage the employ- common neural and cognitive mechanisms for reading ment of music as a technique for literacy remediation. and music abilities that may operate, at least in part, via Musical training during early childhood may be parti- corticofugal shaping of sensory function. By way of audi- cularly important for the advancement of music and tory brainstem spectral enhancement of predictable reading aptitude. Although the music test employed here speech and auditory working memory/attention, music is thought to measure music aptitude, being one’s inher- skill predicts approximately 40% of the variance in read- ent ability for music, the creator of this measure, Edwin ing performance. Definition of common neural and cog- E. Gordon, has long emphasized the impact of music nitive mechanisms for music and reading skills may education during early childhood on music aptitude support the usefulness of music for promoting child lit- scores. Gordon makes this claim in light of his extensive eracy, with the potential to improve the efficacy of reme- longitudinal work showing that music aptitude can dial attempts. improve with musical training, particularly during early childhood [92]. The importance of an early onset of Appendix A music activities is more directly supported by outcomes Grouping according to good and poor music aptitude from neuroscientific research, in which many of the neu- The extent of brainstem enhancement of predictable th roplastic changes associated with musical training are speech in subjects with high (IMMA ≥70 percentile; n = th more extensive in individuals who began training earlier 18) and low (IMMA ≤30 percentile; n = 9) music apti- in their lifetimes [71,72,93-96]. With regard to auditory tude patterned with the results observed when subjects brainstem processing, we found that ABRs in young were divided into good and poor readers. A 2 (condition) adult musicians who began musical training prior to age × 2 (music group) × 2 (harmonic) RMANOVA demon- 7 were distinct from those in musicians who began train- strated an interaction between condition and music ing between the ages of 7-13 [72,93]. Whereas musicians group (F = 6.17, p < 0.02). Post-hoc Mann Whitney U- who began training prior to age 7 demonstrated tests demonstrated that subjects with high music aptitude enhanced ABRs to the spectral components of communi- have a greater enhancement of the second harmonic of cation sounds compared to nonmusicians, those who speech presented in the predictable condition compared began later in life did not. Observations such as this to the variable condition than subjects with low music reflect a critical period for musical training-associated aptitude (H : z = -1.96, p < 0.05; H : z = -1.29, p = 0.19). 2 4 neural plasticity [97] and may speak to the importance of initiating musical training during early childhood for Acknowledgements bringing about the greatest impact on music aptitude or, This work is supported by the National Science Foundation grant 0921275 we propose, reading ability. to NK and the National Institutes of Health grant F31DC011457 to DS. It remains undetermined whether reading abilities are Author details impacted alongside music aptitude with musical training 1 Auditory Neuroscience Laboratory, Northwestern University, Evanston, IL, during childhood or whether the neural mechanism USA. Institute for Neuroscience, Northwestern University, Chicago, IL, USA. Department of Communication Sciences, Northwestern University, Evanston, reported here is affected by musical training. Also undeter- IL, USA. Department of Neurobiology and Physiology, Northwestern mined is whether relationships between music and reading 5 University, Evanston, IL, USA. Department of Otolaryngology, Northwestern work in reverse, with language-based literacy remediation University, Chicago, IL, USA. leading to improved music aptitude. More work (notably, Authors’ contributions longitudinal work) is necessary in order to define relation- DS collected the data, conducted and interpreted the statistical analyses and ships between music aptitude, literacy and the auditory prepared the manuscript. JH collected and processed the data, provided consultation with respect to statistical methods and reviewed the drafts of brainstem response to speech as well as to determine the the manuscript. NK oversaw all aspects of the study and reviewed the drafts impact of formal training, the efficacy of specific training of the manuscript. All authors read and approved the final manuscript. approaches and/or literacy remediation programs. Competing interests The authors declare that they have no competing interests. Conclusions Reading relies on a complex and multifaceted combina- Received: 12 May 2011 Accepted: 17 October 2011 Published: 17 October 2011 tion of processes that have proven difficult to disentangle. 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Russo NM, Nicol TG, Zecker SG, Hayes EA, Kraus N: Auditory training improves neural timing in the human brainstem. Behav Brain Res 2005, • Inclusion in PubMed, CAS, Scopus and Google Scholar 156:95-103. • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit

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