Stimulus and recording

Fig. 1.

Subcortical response of bilinguals (red) and monolinguals (black) to the speech sound [da] presented in multitalker babble. (A) Bilinguals show a larger auditory brainstem response relative to monolinguals. (B) Amplitudes of the individual component frequencies in the steady-state (60–180 ms) region of the response to [da] in multitalker babble. Thin lines represent 1 SEM. Inset in B displays the mean amplitude (±1 SE) of the fundamental frequency in quiet and in multitalker babble for bilinguals and monolinguals. For monolinguals, there is a decrease in the amplitude of the fundamental frequency (F0, 100 Hz) when the stimulus is presented in multitalker babble relative to when it is presented in quiet. In contrast, bilinguals show virtually no change in F0 amplitude between the two conditions. Asterisks represent significance levels: ** P < 0.005, *** P < 0.0001.

Sustained Selective Attention.

 

A multivariate ANOVA was used to identify group differences in performance on the three output measures of the attention paradigm (auditory attention, visual attention, full-scale attention). There was a main effect of group (F = 3.246, P = 0.031) with bilinguals outperforming monolinguals on the auditory (F = 9.234, P = 0.004), visual (F = 5.401, P = 0.025) and full-scale (i.e., collapsed across sensory modalities F = 9.53, P = 0.003) measures of sustained selective attention (Fig. 2).

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Fig. 2.

Performance on the behavioral measure of sustained selective attention and its correlation with subcortical processing in multitalker babble. Bar graphs: Bilinguals (red) outperform monolinguals (black) on sustained selective attention, regardless of sensory domain. Scatter plot: Auditory attention performance was correlated with the F0 encoding in six-talker babble. Asterisks represent significance levels: * P < 0.05, ** P < 0.005.

Correlations Between Sustained Selective Attention and Electrophysiology.

 

To further investigate the effects of bilingualism in the auditory domain, correlations were run on performance on the auditory attention task and neural encoding of the F0 in quiet and in multitalker babble. Although auditory attention did not correlate with F0 amplitude in quiet (r = 0.254, P = 0.081), neural encoding of the F0 in multitalker babble was positively correlated with sustained selective auditory attention (r = 0.442, P = 0.002) as can be seen in Fig. 2. When performing separate correlations for the two languages groups, the correlation held for the bilingual group (r = 0.483, P = 0.02), but not the monolingual group (r = 0.09, P = 0.668), further supporting the notion that bilingual experience is what drives the relationship between F0 encoding and auditory attention.

Additionally, in the visual domain, the same pattern was seen, such that visual attention did not correlate with F0 amplitude in quiet (r = 0.263, P = 0.071), but did correlate with F0 amplitude in multitalker babble (r = 0.393, P = 0.006). Again, this relationship was driven by bilingual (r = 0.482, P = 0.020), but not monolingual (r = −0.136, P = 0.581), performance.

Discussion

This study establishes a neural signature of bilingual experience, whereby bilinguals, relative to monolinguals, have enhanced subcortical representation of the F0 to a target sound presented in a noisy background coupled with heightened sustained selective attention. We argue that enhanced processing of sound and its relationship to attention reveal a biological basis for enhanced flexibility and efficiency of auditory processing in bilinguals. Our findings, combined with previous work, suggest that the bilingual brain undergoes widespread neural specialization that encompasses subcortical and cortical structures relating to language and cognitive processing (7, 8, 37⇓–39). This neural specialization likely results from the bilingual’s complex linguistic environment, including a rich diversity in phonetic, phonological, and grammatical structure both within and between talkers. The relationship between sustained attention and subcortical encoding of F0 is a compelling demonstration of experience-dependent plasticity, especially given that there is no correlation between these two measures within the monolingual group. Indeed, these sensory and cognitive changes may be driven synergistically within the bilingual neural system. This is because both robust representation of the F0 and sustained attention are required for accurate perception of auditory events in our acoustically dynamic world; however, the need for well honed sensory and cognitive processes may be higher in a bilingual’s phonologically rich and cognitively demanding soundscape.

In bilinguals, immersion in an enriched environment may strengthen attention directed to all linguistic stimuli. With continued exposure, their heightened attention becomes increasingly focused on the behaviorally-relevant stimulus features, such as the F0. Subsequently, the auditory system becomes tuned to automatically process sound more efficiently, as seen here in the cABR. This tuning is likely driven by an interplay of bottom-up and top-down influences, where top-down attentional processes target the most behaviorally relevant features of the stimulus, and the complexity of the bilingual’s linguistic input strengthens bottom-up processing. Thus, we maintain that enriched linguistic experience, coupled with experience-related tuning of attention, leads to advantages in the neural encoding of specific sound features that are important in daily communication rather than a general gain in the neural processing of all aspects of sound.

The bilingual’s rich linguistic environment may include slight changes in F0 profile, which occur when a bilingual speaker switches between languages (40). Such subtle F0 differences might provide a more dynamic listening environment for a bilingual than a monolingual, especially given that bilingual communication can often involve language switching. The added signal variability could mark the F0 as an important language-specific cue for bilinguals, which may contribute to the enhancements in sound processing seen in the current study. Thus, for a bilingual listener, the F0 may convey relevant linguistic information beyond what is important to a monolingual listener. By virtue of speaking and listening in two languages, bilinguals experience an enriched linguistic environment relative to monolinguals, and the active manipulation of linguistic complexity confers advantages in the auditory and executive systems of bilinguals.

The results of the current study are consistent with the OPERA (Overlap, Precision, Emotion, Repetition, Attention) hypothesis, which was originally developed to describe learning-related plasticity that occurs with musical training (41). Within the OPERA framework, attention is critical for robust learning, such that changes in the cABR require active engagement with sound (41). This subcortical tuning likely results from a dynamic feedback system that includes both sensory and cognitive mechanisms interacting via bottom-up and top-down mechanisms (23). The OPERA hypothesis is corroborated by animal work showing that sound-to-meaning associations drive neural plasticity (3, 42, 43) and that feedback from cortical areas is necessary for learning-related plasticity in subcortical regions (44). Thus, we propose that in humans, cognitive skills, including attention, may drive experience-dependent neural plasticity for behaviorally meaningful stimuli. These enhanced top-down connections may also promote bottom-up processing, which then combine to produce gains in sensory processing that are observed in auditory experts, such as bilinguals and musicians.

Similar to bilinguals, musicians demonstrate neural and cognitive advantages in processing of auditory stimuli (33, 45). In musicians, training on complex sound through explicit music instruction and practice leads to enhanced acoustic encoding that generalizes across the musical and linguistic domains (28, 33, 41, 45). However, in contrast, bilingual auditory training is more implicit; advantages in executive function and neural enhancements in auditory processing are conferred through daily exposure to multiple sound sets (i.e., languages) (31). Here, we discover that language learning, like more explicit music instruction, also impacts subcortical sound processing. This enhanced neural representation of the auditory signal may facilitate learning a new language, a skill in which bilinguals outperform monolinguals (46). Indeed, musicians, who show neural enhancements similar to bilinguals, also appear to be better able to detect acoustic cues in foreign speech relative to nonmusicians (32, 45, 47).

In conclusion, we provide evidence that continuously manipulating sounds across two languages leads to an expertise in how sound is encoded in the bilingual brain. The neural enhancements observed in multitalker babble intersect with bilinguals’ known advantages in cognitive control and are similar to advantages seen in musicians. In both groups of auditory experts (i.e., musicians and bilinguals), enhanced experience with sound results in an auditory system that is highly efficient, flexible and focused in its automatic sound processing, especially in challenging or novel listening conditions. Thus, converging evidence from both musicians and bilinguals points to subcortical plasticity as providing a biological basis for advantages in real-world experiences with sound.

Materials and Methods

Subjects.

 

Subjects were 48 incoming freshmen attending three public high schools in Chicago, IL. Inclusionary criteria included, normal IQ (Wechsler Abbreviated Scale of Intelligence, WASI; bilinguals: 98.95 ± 8.12; monolinguals: 97.7 ± 11.1; F = 0.200, P = 0.657), normal hearing defined as air conduction thresholds < 20 dB normal hearing level (nHL) for octaves from 125 to 8,000 Hz, with no apparent air-bone conduction gap, click-evoked brainstem response latencies within normal limits [the 100-μs click stimulus was presented at 80 dB sound pressure level (SPL) at a rate of 31 per s], and no external diagnosis of an attention disorder (ADHD or ADD). Monolinguals (n = 25; 52% female) and Spanish–English bilinguals (n = 23; 56.5% female) were matched on age (bilinguals: 14.8 ± 0.54 y; monolinguals: 14.6 ± 0.46 y; F = 2.801, P = 0.101) and socioeconomic status (SES) based on maternal education (48) such that 52% of monolingual families and 65% of bilingual families reported between middle school and senior year of high school as the highest maternal education.

Language proficiency was measured by the Language Experience and Proficiency Questionnaire (LEAP-Q, ref. 49). To be included in the study, all subjects had to report high English proficiency (≥8 out of 10 for the average self-report of English speaking and understanding proficiency, monolinguals: 9.32 ± 0.8; bilinguals 9.36 ± 0.6). Spanish–English bilinguals additionally had to report high Spanish proficiency (≥8 out of 10 for the average self-report of Spanish speaking and understanding proficiency; 8.36 ± 0.8). The bilingual subjects also reported speaking and learning Spanish at home (100% of bilinguals spoke Spanish at home; 78% also reported speaking English at home), and their parents/guardians reported that the child spoke two languages. The bilingual subjects were all early bilinguals; their age of first exposure was about 3 y of age (50) for both languages (Spanish: 3.04 ± 2 y; English 3.47 ± 2 y). Of the bilingual subjects, 61% identified Spanish as their native language, whereas 39% considered English their native language.

Monolingual subjects reported no exposure to a second language and their parents also reported that the child only knew English. In the monolingual group, 12 (6 female, 7 low socioeconomic standing) of the subjects were of Hispanic descent. The remaining 13 subjects self-identified as African American (n = 11; 6 female, 5 low socioeconomic standing) or Caucasian (n = 2; 1 female, 1 low socioeconomic standing). Within the monolingual group, the Hispanic and non-Hispanic subgroups did not differ on any of the measures that were analyzed in the current study (WASI P > 0.250; full-scale sustained selective attention P = 0.161; auditory sustained selective attention P > 0.250; visual sustained selective attention P = 0.081; F0 amplitude in quiet P > 0 0.250; F0 amplitude in six-talker babble P > 0.250). Given that the groups did not differ on these measures, the results seen in the current study cannot be driven by ethnic or cultural differences between the monolingual and bilingual groups. Because all subjects in the bilingual group were of Hispanic descent, this subanalysis was not performed in this language group.

Sustained Selective Attention.

 

Sustained selective attention was assessed by the Integrated Visual and Auditory Continuous Performance Test (IVA+Plus, www.braintrain.com), a 20-min test with 500 trials of 1s and 2s presented in a pseudorandom order to the visual and/or auditory modalities. For this test, the subject clicks the mouse only when a 1 (but not a 2) is seen or heard. The subject’s responses during the test capture abilities of attention, control, and focus, both collectively and individually within the auditory and visual domains. Responses were converted to age-normed standard scores. To assess sustained selective attention in an ecologically valid setting, subjects were administered this test over headphones at their high school using a laptop computer that was placed 60 cm from the participant.

Electrophysiological Recording.

Stimulus and recording.

 

Stimulus and recording parameters followed those described in ref. 23. The complex stimulus [da] is a dynamic, six-formant, 170-ms sound synthesized at a 20-kHz sampling rate using a Klatt synthesizer (51). Except for the initial 5-ms stop burst, this syllable is voiced throughout with a steady fundamental frequency (F0 = 100 Hz). This stimulus is characterized by a 50-ms formant transition (transition between [d] and [a]) followed by a 120-ms steady-state [a] portion during which the formants are unchanging. The [da] stimulus was presented 6,300 times with an 81-ms interstimulus interval presented in alternating stimulus polarities to the right ear at 80-dB SPL through an insert earphone (ER-3; Etymotic Research) using the stimulus presentation software NeuroScan Stim2 (Sound module; Compumedics). Responses, which originate primarily from the inferior colliculus (52), were differentially recorded in a sound-attenuated, electrically-shielded chamber using NeuroScan Acquire4 at a sampling rate of 20 kHz. Ag/Ag-Cl electrodes were applied in a vertical montage from Cz-to-earlobe with forehead as ground. During electrophysiological testing, the participant watched a movie of his or her choice in a comfortable reclining chair. The left ear was unoccluded enabling the participant to hear the movie soundtrack played at <40 dB SPL, an insufficient intensity to mask the stimulus. The [da] was presented alone and in the context of multitalker babble. The multitalker babble (four female and two male voices) was created by mixing six tracks of English nonsense sentences in Cool Edit Pro, version 2.1 (Syntrillium Software, 2003), into a 45-s duration babble track that was presented at a signal-to-noise (SNR) of +10 dB relative to the [da] based on the root mean square (RMS) amplitude of the entire track.

Data averaging.

 

For both the quiet and babble conditions, electrophysiological responses were off-line bandpass filtered in Neuroscan Edit from 70 to 2,000 Hz (12 dB/octave, zero phase-shift) to include energy within the phase-locking limits of the inferior colliculus (52, 53) and to minimize low-frequency myogenic noise and cortical activity. Responses were then averaged over a −40- to 190-ms window, with stimulus onset occurring at time 0. An artifact reject criterion of ±35 μV was applied, resulting in prestimulus baseline corrected final averages comprising ~6,000 sweeps.