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Articles, Behavioral/Cognitive

Plasticity in Developing Brain: Active Auditory Exposure Impacts Prelinguistic Acoustic Mapping

April A. Benasich, Naseem A. Choudhury, Teresa Realpe-Bonilla and Cynthia P. Roesler
Journal of Neuroscience 1 October 2014, 34 (40) 13349-13363; DOI: https://doi.org/10.1523/JNEUROSCI.0972-14.2014
April A. Benasich
1Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey–Newark, Newark, New Jersey 07102, and
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Naseem A. Choudhury
1Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey–Newark, Newark, New Jersey 07102, and
2Department of Psychology, School of Social Science and Human Services, Ramapo College of New Jersey, Mahwah, New Jersey 07430
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Teresa Realpe-Bonilla
1Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey–Newark, Newark, New Jersey 07102, and
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Cynthia P. Roesler
1Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey–Newark, Newark, New Jersey 07102, and
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  • Figure 1.
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    Figure 1.

    Overall study design and grand average waveforms depicting maturational effects from 4 to 7 months of age. a, Schematic of overall study design. b, Grand average waveforms from 124 electrodes at Fz at the initial 4 month visit (before auditory exposure) for the AEx and PEx groups, and for both 4 month groups combined. Stimuli were complex tone pairs; each tone was 70 ms in duration with either a 300 or 70 ms within-pair ISI, presented in a standard blocked design. Standard (blue) and deviant (red) waves are shown for the control (300 ms ISI) and fast-rate (70 ms ISI) conditions. No significant differences emerged between the AEx (dotted line) and PEx (dashed line) groups; thus, all the 4-month-old pre-exposure infants (solid line) combined served as the control group for the cross-sectional maturation analyses. c, Grand average waveforms from 124 electrodes at Fz, for the 300 and 70 ms ISI conditions for the 4 month combined pre-exposure group and the 7 month NC group. Standard waves are in blue, and deviant waves are in red. Maturational effects were seen on morphology, amplitude, and latency as a function of age for both conditions on both standard and deviant waves at all (frontal, frontocentral, and central) channels. At 300 ms ISI, significantly faster latencies for the 7 month group compared with the younger infants are seen for the P1 and P2 peaks as well as significantly larger amplitudes on the standard and deviant waves. Similarly, at 70 ms ISI the P1 on the standard waves and the P1 and P2 on the deviant waves in 7-month-old children were significantly faster and smaller in amplitude than those in 4-month-old children. Negative peak amplitudes increased from 4 to 7 months.

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    Figure 2.

    Group effects of auditory exposure on latency and amplitude for all three groups at the 7 month post-test. a, Grand average waveforms from 124 electrodes overlaid for AEx (solid line), PEx (dashed line), and NC (dotted line) groups at Fz. Standard (blue) and deviant (red) waves are shown for the control (300 ms ISI) and fast-rate (70 ms ISI) conditions. b, P2 peak amplitudes for all nine electrodes of interest are shown by group (red, AEx; green, PEx; blue, NC) for each tone of the two tone pairs in the 300 ms ISI condition. The four P2 peaks depicted on the x-axis include the P2 responses to the standard pair (two) and from the predeviant standard (one), as well as the P2 peak elicited by the 1200 Hz deviant tone. The AEx group achieved significantly higher amplitudes for the repeated 8oo Hz standard tones compared with the PEx and NC groups. However, all groups had significantly higher amplitudes for the 1200 Hz deviant tone. Bar graphs (error bars indicate SEM) show the mean P2 peak amplitude for each tone. T1, tone 1; T2, tone 2; solid bars, 800 Hz tones; striped bars, 1200 Hz tone. c, P2 peak amplitudes for all nine electrodes of interest by group (red, AEx; green, PEx; blue, NC) for each of the merged tone pairs in the 70 ms ISI condition. Only two P2 peaks are generated at 70 ms ISI. The NC group had significantly lower amplitudes for both the STD (800–800 Hz) and DEV (800–1200 Hz) merged tones compared with those in the AEx and PEx groups. Bar graphs (error bars indicate SEM) show the mean P2 peak amplitude for each tone. T1, Tone 1; T2, tone2; solid bars, STD; striped bars, DEV.

  • Figure 3.
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    Figure 3.

    Group differences in latency and amplitude at 70 ms ISI among the three groups at the 7 month post-test. a, Grand average waveforms for all 124 electrodes by group are shown at Fz for the P2 peak on the deviant wave. Highlighted yellow bars on the deviant waveform indicate the location of the maximum P2 peak for each group. Time-locked, age-appropriate topograms to the P2 peak latency by group are also shown. The amplitude scale is shown in microvolts; blue represents negative and red positive activity. A red box around a topogram denotes significantly faster latencies. The AEx group is significantly faster than both the PEx and NC groups, and the PEx group is significantly faster than the NC group. b, Grand average waveforms for all 124 electrodes by group are shown at Fz for the N2* on the deviant wave. Highlighted yellow bars on the deviant waveform indicate the location of the maximum N2* peak for each group. Time-locked, age-appropriate topograms to the N2* peak latency for each group are shown. Amplitude is in microvolts; blue represents negative and red positive activity. A red box around a topogram indicates significantly faster latencies. The AEx and the PEx groups are significantly faster than the NC group.

  • Figure 4.
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    Figure 4.

    Group differences in morphology for the 70 ms ISI grand average waveform at the 7 month post-test. a, An exemplar waveform from each of the three 7-month-old groups demonstrates the emergence of additional peaks for the AEx group that are not evident for PEx or NC groups. Emerging double peaks (starred) were seen at the 7 month post-test in the majority (78%) of AEx infants at 7 months of age; 41% of the PEx group and 22% of the NC group (χ2 = 8.6, p = 0.01) exhibited this signature maturational profile. b, Morphologically similar double peaks (starred) seen in typically developing 12- and 24-month-old children. (Grand average waveforms at Fz were adapted from Choudhury and Benasich, 2011; plotted at slightly larger scale to accommodate larger-amplitude peaks of the younger infants.) While the double peaks depicted here for the older children are similar morphologically to those seen in the AEx group, typical maturational differences are present for these 12- and 24-month-old children, including faster latencies and smaller amplitudes are seen compared with the 7-month-old children in a.

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    Figure 5.

    Generalization to nonexposed stimuli in the multideviant paradigm by group at the 7 month post-test: enhanced processing on the standard wave. a, Grand average waveforms for all 124 electrodes at Fz by group to the STD stimulus in the multideviant generalization paradigm. The P1 peak for the STD waveform is significantly faster for the AEx group (solid line) than for the PEx (dashed line) and NC (dotted line) groups. b, Bar graphs (error bars indicate SEM) depicting significantly faster latency of P1 for the STD in the multideviant generalization paradigm for the AEx group (left) when compared with PEx and NC groups. The AEx group also demonstrated smaller, more mature amplitudes for the P1 and N1 peaks compared with those in the PEx and NC groups. All values are plotted from the mean grand averages at Fz.

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    Figure 6.

    Generalization to nonexposed stimuli in the multideviant paradigm by group at the 7 month post-test: enhanced processing on P1 and N1 for all three deviants. a, Bar graphs depict the mean latency of each DEV at each of the nine electrode sites by group. Significantly faster P1 latencies (p < 0.05) are seen for the AEx group (red) for all three deviants and for all nine electrode sites compared with those in the PEx (green) and NC (blue) groups. Significant differences are circled. b, Bar graphs (error bars indicate SEM) show the mean latency of each group by DEV type (gap, duration, frequency). There were significant group interactions for N1 latency. For each deviant, the AEx group was significantly faster at all electrode sites than the PEx and NC groups (p values < 0.05). A significant interaction revealed that the NC group was significantly slower when processing the frequency deviant. All values are plotted from the mean grand averages at F3.

  • Figure 7.
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    Figure 7.

    Generalization to nonexposed stimuli in the multideviant paradigm at the 7 month post-test: subgroup differences in the P2–N2 complex on the gap deviant. a, Grand average waveforms for 124 electrodes at Fz to the gap generalization stimulus for all three groups (AEx, PEx, and NC) combined, sorted by P2–N2 subgroup (presence/absence of a P2–N2 complex in the 250–550 ms window). Standard (blue), deviant (red), and difference (green) waves are shown for the gap deviant stimulus. A P2–N2 complex was identified in 71% of the AEx group, 41% of the PEx, and 30% of the NC infants. The AEx group significantly differed from the NC group (χ2 = 4.0, p < 0.05); the PEx and NC groups did not differ from each other (χ2 = 1.8, p = 0.18). b, Grand average waveforms for 124 electrodes at Fz to the gap generalization stimulus for two groups (AEx and NC) combined, sorted by P2–N2 subgroup (absence of P2–N2 vs presence of P2–N2). Standard (blue), deviant (red), and difference (green) waves are shown for the gap deviant stimulus. Significant interactions were seen for all nine electrode sites examined (range, F(1,20) = 5.2–10.8, p < 0.03). Infants in the AEx group who showed the P2–N2 complex had significantly faster latencies and showed better discrimination (i.e., significantly larger mismatch response amplitudes) when compared with those infants who did not show the P2–N2 complex (range, F(1,20) = 5.2–16, p < 0.03).

Tables

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    Table 1.

    Time window ranges for peak extraction

    PeakAEx groupPEx groupNC group
    PretestPost-testPretestPost-testPretestPost-test
    300 ms ISI paradigm
        P1T1140–210120–190160–230120–200110–190
        N1 T1240–300200–270240–320200–280200–270
        P2T1300–370260–330320–370280–340270–340
        N2T1380–450350–430370–430340–430370–440
        P1T2430–470 (60–100)430–540 (60–170)430–500 (60–130)430–530 (60–160)440–500 (70–130)
        N1 T2470–540 (100–170)540–600 (170–230)500–560 (130–190)530–620 (160–250)500–600 (130–230)
        P2T2540–650 (170–280)600–700 (230–330)560–670 (190–300)620–720 (250–350)600–730 (230–360)
        N2T2650–740 (280–370)700–800 (330–430)670–680 (300–310)720–810 (350–440)730–830 (360–460)
    70 ms ISI paradigma
        P1170–240130–220170–240120–220130–220
        N1/N2*260–340 (120–200)220–360 (80–220)270–370 (130–230)220–420 (80–280)250–360 (110–220)
        P2340–430 (200–290)290–470 (150–330)370–430 (230–290)420–510 (280–370)320–470 (180–330)
    Multideviant paradigm
        P180–14090–160100–160
        N1150–220160–230170–230
        P2230–300230–320240–320
        N2350–440320–440360–460
    • Latencies reported here are absolute values (from zero); relative values (from the second tone of the tone pair) are reported in parentheses. The time window ranges include both STD and DEV waveforms.

    • ↵aNegative peak labels N1/N2* refer to the standard wave (N1)/deviant wave (N2*) peaks, respectively.

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    Table 2.

    Summary table of results

    ConditionIndependent variablesDependent variablesTestResults
    Maturation: cross-sectional300 ms ISI tone pair4- and 7-month-old cross-sectional age groups4 months: P1, N1, P2, N2
    7 months: P1, N1, P2, N2 (to tone 1); P1T2, N1T2, P2T2, N2T2, (to tone 2)
    Independent t testSignificantly faster and larger P1 to tone 1 response for 7-month-old group compared with younger group
    70 ms ISI tone pair4- and 7-month-old cross-sectional age groups4 and 7 months: P1, N1, P2Independent t testSignificantly faster and smaller P1 and P2 responses for 7-month-old group compared with younger group
    Significantly bigger negative peaks for 7-month-old children
    Group differences
        Amplitude and latency differences300 ms ISI tone pair7-month-old AEx, PEx, and NC groupsFour P2 peaks (2 from the standard pair, 1 from the pre-deviant standard and 1 from the deviant tone of the target pair)3 × 4 factorial ANOVASignificantly larger P2 response for the deviant tone (1200 Hz) for all 3 groups
    The AEX group had significantly bigger P2 responses for the oft-repeated 800 Hz tone
    70 ms ISI tone pair7-month-old AEx, PEx, and NC groupsTwo P2 peaks (1 from standard and 1 from deviant tone)3 × 2 factorial ANOVASignificantly smaller P2 responses for the NC group compared with the AEx and PEx groups
    70 ms ISI tone pair7-month-old AEx, PEx, and NC groupsN2* and P2 peaks of deviant waveOne-way ANOVAThe AEx and PEx groups have significantly faster N2* and P2 responses
    The AEx group had significantly larger N2* peak responses
        Morphological differences70 ms ISI tone pair7-month-old AEx, PEx, and NC groupsPresence vs absence of new emerging peaksχ2A majority of infants in the AEx group showed the presence of emerging peaks
    Generalization
        Multideviant paradigmMultideviant paradigm7-month-old AEx, PEx, and NC groupsP1 and N1 peaks of the standard waveOne-way ANOVAThe AEx group had significantly faster P1 peak responses and more mature P1 and N1 responses
    Multideviant paradigm7-month-old AEx, PEx, and NC groupsP1 and N1 peaks for the 3 deviants3 × 3 factorial ANOVAThe AEx group had significantly faster P1 peak responses
    Significant interactions for N1 peak responses where the NC group was notably slower compared to the other two groups
        Gap deviantGap deviant of multideviant paradigmAEx group vs NC groupPresence vs Absence of P2–N2 complexχ2The AEx group significantly differed from the NC group while there was no significant difference between PEx and NC groups
    PEx group vs NC group
    Gap deviant of multideviant paradigmGroup (AEx vs NC) vs subgroup (presence of P2–N2 complex vs absence of P2–N2 complex)N2 peak response2 × 2 ANOVASignificant interactions found where the AEx group that showed the P2–N2 complex had faster latencies as compared to their naive peers
    Gap deviant of multi-deviant paradigmGroup (AEx vs NC) vs subgroup (presence of P2–N2 complex vs absence of P2–N2 complex)MMR (mismatch response)2 × 2 ANOVAInfants that showed the P2–N2 complex had significantly larger MMR responses compared with those infants who did not show the P2–N2 complex
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Plasticity in Developing Brain: Active Auditory Exposure Impacts Prelinguistic Acoustic Mapping
April A. Benasich, Naseem A. Choudhury, Teresa Realpe-Bonilla, Cynthia P. Roesler
Journal of Neuroscience 1 October 2014, 34 (40) 13349-13363; DOI: 10.1523/JNEUROSCI.0972-14.2014

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Plasticity in Developing Brain: Active Auditory Exposure Impacts Prelinguistic Acoustic Mapping
April A. Benasich, Naseem A. Choudhury, Teresa Realpe-Bonilla, Cynthia P. Roesler
Journal of Neuroscience 1 October 2014, 34 (40) 13349-13363; DOI: 10.1523/JNEUROSCI.0972-14.2014
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Keywords

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