- Email: [email protected]
Dichotic listening in children: Age-related changes in direction and magnitude of ear advantage
Brain and Cognition 76 (2011) 316–322
Contents lists available at ScienceDirect
Brain and Cognition journal homepage: www.elsevier.com/locate/b&c
Dichotic listening in children: Age-related changes in direction and magnitude of ear advantage Deborah W. Moncrieff ⇑ University of Pittsburgh, 4033 Forbes Tower, Pittsburgh, PA 15260, United States
a r t i c l e
i n f o
Article history: Available online 6 May 2011 Keywords: Dichotic Ear advantage Lateralization Development Children Amblyaudia
a b s t r a c t Children between the ages of 5 and 12 years were tested with dichotic listening tests utilizing single syllable words and random presentations of digits. They produced a higher prevalence of left ear dominance than expected, especially among right-handed children when tested with words. Whether more children demonstrate the LEA because of right hemisphere dominance for language or because there is less stability in ear advantage direction at younger ages cannot be fully resolved by this study. When ear advantages were measured by subtracting each child’s lower score from the higher score without regard to right or left direction, an age-related trend toward lower measures of ear advantage was evident. This trend was greater for dichotic words than for dichotic digits. Structural factors that may be related to these results and possible influences of attention and verbal workload on the two kinds of dichotic stimuli are discussed. Ó 2011 Elsevier Inc. All rights reserved.
1. Introduction We measure hearing one ear at a time, but listening occurs through both ears and complete parity of signals arriving at the right and left ear at any given time is relatively rare. Therefore, the intake of information through the auditory system requires an online integration of differing and potentially competing information presented to the two ears. Broadbent (1954) first reported that when two different words were presented to the right and left ear simultaneously, normal listeners could accurately identify more words heard at their right ear. Later, Doreen Kimura (1961) ascribed the dichotic listening right ear advantage (REA) to stronger crossed auditory pathways from the right ear ascending directly to the speech-dominant left cerebral hemisphere. She further noted that the REA was enhanced by suppression of information ascending via the ipsilateral pathway from the left ear to the speech-dominant left hemisphere. At the time, researchers were concerned that handedness may not be an accurate index of hemispheric dominance for language (Goodglass & Otjadfasel, 1954) and they saw the dichotic listening ear advantage as a potentially better method for determining lateralization. Shortly after her groundbreaking study of dichotic listening in adults, Kimura (1963) reported that right-handed children from age 4 to 9 years produced an average REA, suggesting a contralateral left hemisphere lateralization for speech stimuli as early as age 4 years or before. She also noted that cerebral dominance
⇑ Fax: +1 412 383 6555. E-mail address: [email protected] 0278-2626/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2011.03.013
may not be rigidly established in younger children, beginning a controversy over development of ear advantage and language lateralization that persists today. Bryden (1970) reported that the prevalence of an REA increased from 2nd to 6th grade among right-handers, suggesting that left hemisphere dominance for language may not be firmly established in younger children. He also reported that some left-handers switched to a left-ear advantage (LEA) by the 6th grade, raising the possibility that direction of ear advantage is subject to developmental factors and that right hemisphere dominance may also be normal. Some reported that the magnitude of the REA changed with age as children became more strongly lateralized for language (Fennell, Satz, & Morris, 1983) but others reported that the REA remained the same when tested with consonant–vowels (CVs) (Berlin, Hughes, Lowe-Bell, & Berlin, 1973), words (Geffen, 1976), or CVs, words, and digits (Bryden & Allard, 1981). A statistical analysis of two longitudinal studies utilizing dichotic digits in school-age subjects found no developmental pattern and concluded that dichotic listening in the free recall mode may be ineffective for measuring lateralization (Morris, Bakker, & Satz, 1984). This prompted a flurry of research into response techniques to add control over the listener’s attention, but these also failed to produce a reliable pattern of development. For many decades, researchers interested in development of cerebral dominance and its impact on language and learning have used the dichotic listening technique to investigate these issues. With digits, words, and CVs, they have compared free recall and directed response methodologies, and have asked children to respond by recognition, memory, or repetition techniques. Some have reported a larger REA in children with disabilities when
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
tested with digits and words because of lower reports of stimuli from the left ear (Kershner & Morton, 1990; Moncrieff & Black, 2008; Morton & Siegel, 1991) whereas others reported a weaker REA or the LEA when children with disabilities were tested with CVs (Helland & Asbjornsen, 2001; Martínez & Sánchez, 1995; Moncrieff & Black, 2008; Morton & Siegel, 1991; Obrzut, Conrad, & Boliek, 1989). Some dichotic listening tests with words and digits have been administered to children from age 5 to age 18 for the purpose of establishing normative data so that the tests can be administered clinically. Normative information is available as separate right and left ear scores and test results are compared to standard values to determine if one or both ears fall below normal (Katz, Basil, & Smith, 1963; Moncrieff & Wilson, 2009; Musiek, 1983). Average values of the REA and the overall prevalence of the LEA at each age level in normative studies are typically not reported, but there does appear to be a decrease in magnitude of the REA when children are tested with digits and words, but not when they are assessed with CVs. A recent study compared the incidence of abnormal results when magnitude of the REA was used instead of standard scoring techniques and reported that ear advantage magnitude may be more effective at determining clinically significant results than individual or combined ear scores when assessing children’s dichotic listening (Moncrieff, 2004). Additional information about direction and magnitude of ear advantage could reveal age-related trends in development of dichotic listening skills. Normative values for ear advantage based on the absolute difference between the two ears without regard to right or left might be more useful in determining clinically significant outcomes in children. Current normative data fails to account for inclusion of left-ear dominance among children tested. Therefore, a true measure of ear advantage at each age could be underestimated. Long ago, Larsen (1984) suggested that stable ear advantage values in young children may be due to the customary practice of determining them by subtracting the left ear score from the right ear score. If younger children produce larger ear advantages and several produce the LEA, the presence of LEA data yields negative values that when added to the positive values for REAs would yield lower averages across children within that age group. Larsen reported that when differences between the two ears were calculated for each individual child, developmental patterns emerged. Similarly, absolute values for ear differences could provide important evidence of how the magnitude of ear advantage changes with development. Information about age-related prevalence of the LEA would also address whether direction of ear advantage changes with maturity, with some children switching from LEA to REA. A consistent REA prevalence, similar to the reported 80–85% of right-handed adults and 50% of left-handed adults (Hiscock, Inch, & Ewing, 2005), would support the notion that hemispheric dominance is fully lateralized at birth. In contrast, if ear advantage direction depends on developmental factors, then REA prevalence could increase or decrease as children mature. Bryden’s (1970) report of a higher prevalence of the LEA among younger children suggested that direction of ear advantage may be unstable among younger children and that some switch from the LEA to the REA as a consequence of normal development. Two new dichotic listening tests have been developed and normative information is currently being gathered from school-age children. A preliminary review of results from this data collection will be reported here to explore whether direction and degree of ear advantage are stable across school-age development. Stability of ear advantage direction will be confirmed if the prevalence of the REA and the LEA remains similar across all age levels. Increases in prevalence of either the REA or LEA would support the notion
317
that developmental increases in attention, working memory and/ or language skills affect ear advantage direction. Finally, because the magnitude of ear advantage may be underestimated at each age level by numerically averaging across children with both REAs and LEAs, ear advantages will also be calculated as the numerical difference between the dominant and non-dominant ear without regard to right or left. Age-related changes in ear advantage using both the traditional method and this alternative method will be examined for developmental trends and the two methods will be compared for significant differences.
2. Methods Children ages 5–12 years participated in the study. Most were recruited for a normative study and others were assessed as part of a clinical evaluation for auditory processing (23 of the 50 children evaluated clinically were thought to have greater than normal difficulty with dichotic listening). Results from both classes of children are included in this study because it is not intended as a normative sample per se but is interested in magnitude and direction of ear advantage within individual age groups. Each child participated with the consent of a parent or legal guardian in accordance with policies of the university institutional review board or the clinical site at which they were assessed. Children were tested at various locations, including a quiet room at their school or home, at a hospital, at a clinical practice, or at a university research laboratory. All children had normal hearing with no pure tone thresholds poorer than 20 dB HL in either ear at the time of testing. Handedness was assessed by a modified survey which asked about use of everyday items such as a toothbrush, pen for writing a letter, or scissors (Annett, 1970). In some cases, handedness was not assessed. Two different dichotic listening tests were used. Normative data for one of the tests, the Randomized Dichotic Digits Test (RDDT), has been previously reported for children ages 10 to 18 years (Moncrieff & Wilson, 2009). The RDDT lacks the ceiling effects that have been found among older children when tested with double dichotic digits (Moncrieff & Musiek, 2002; Neijenhuis, Snik, & van den Broek, 2003). The Dichotic Words Test (DWT) is a new dichotic listening test comprised of single syllable words. Stimuli for the DWT were created by aligning two single syllable words spoken in a male voice, each matched for time of onset and time of offset so that the total duration of each word in a pair was identical. Four lists of 25 words were created so that each list was balanced for phonemic content. The initial and final consonant and medial vowel were balanced to the extent possible within each list and across the four lists. Average root mean square (RMS) amplitude was equalized for each word so that all stimuli were presented at the same RMS amplitude across the entire test. Digits and words were presented at a comfortable listening level to the two ears, either at 50 dB HL bilaterally through insert earphones or TDH-50 supra-aural earphones attached to a clinical audiometer or through Sennheiser 280 Pro circumaural earphones attached to a Dell laptop computer with output level confirmed by the examiner prior to beginning the test. Each time, the intensity was balanced across the two ears so that the presentation to the right ear was always at the same intensity as the presentation to the left ear. Children were instructed to listen for the digits or words and to repeat everything that they had heard from each ear. All children completed two word lists and the randomized list of digits in a free recall paradigm in which they were given no specific instructions about the order for reporting what they heard. A subset of children also completed two other lists of the DWT in a directed response format during which they were instructed to repeat the word heard in their right ear first for one list and the word heard in their left ear first for another list. The number of correct
318
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
responses was converted to percentage for the 1-pair, 2-pairs and 3-pairs conditions of the RDDT and across each list of the DWT. DWT lists were chosen randomly from among the four lists available for each child tested. Ear advantages were measured two ways. In the first traditional way, the score for the left ear was subtracted from the score for the right ear which yields a positive number for a REA, a negative number for a LEA, and zero for no ear advantage (NEA). Results were used to measure the prevalence of ear advantage directions and to produce an average value among children in each age group. In the second case, the lower score was subtracted from the higher score to yield an ear advantage that provides the difference between the child’s dominant and non-dominant ears without regard to right or left. Again, an average value for ear advantage was measured for the children within each age group. The two average values for ear advantage were compared for significant differences. 3. Results A total of 247 children were tested with the RDDT and 241 children were tested with the DWT in the free recall format. Among
Table 1 Demographics regarding the number of male and female children at each age level included in the study and indicating their handedness if known. Age
Males L-Hand
Females R-Hand
Total
Unknown
L-Hand
R-Hand
Unknown
1 2 1 2 5 4 4 3 22
1 1 1 0 1 0 1 0 5
5 10 19 11 11 8 22 15 101
0 1 5 4 1 1 3 2 17
14 26 39 35 28 20 49 30 241
Randomized dichotic digits test 5 1 4 0 6 1 8 1 7 1 9 1 8 1 14 2 9 0 6 3 10 0 11 7 11 4 25 9 12 0 17 4 Total 8 94 27
0 1 0 0 1 0 1 1 4
4 7 9 10 7 12 27 20 96
0 0 5 4 1 1 5 2 18
9 18 25 31 18 31 71 44 247
Dichotic words test 5 1 6 6 1 11 7 1 12 8 1 17 9 1 9 10 0 7 11 2 17 12 0 10 Total 7 89
those tested with the DWT, some were also tested in the directed response format (n = 145). A paired t-test on DWT ear advantages between the free recall and directed response formats among those who were tested both ways showed no significant differences in ear advantages, t = .586, p = .559, so scores for the two free recall lists of the DWT were used for determining ear advantages in this study. Another paired t-test on differences in RDDT ear advantages between the 2-pairs condition and the overall test also failed to achieve significance, t = 1.905, p = .058, so scores for the 2-pairs condition of the RDDT were used. Demographics regarding age, gender, and handedness of children involved in the study are shown in Table 1. A total of 190 children tested with the RDDT were right-handed (96 females and 94 males) and similarly, 190 of the children tested with the DWT were right-handed (89 females and 101 males). Ear advantages were compared between right-handed children and all other children in the study (left-handed and handedness unknown) by univariate analysis of variance (ANOVA) and no significant differences in ear advantages were noted for the RDDT, F(1, 246) = 1.902, p = .169, or the DWT, F(1, 240) = 1.370, p = .243. As shown in Table 2, the only significant main effect on ear advantage when children were tested with the DWT occurred for gender because the average overall REA was greater among males than females (see Fig. 1). Age failed to produce any significant effects on DWT ear advantages. There were significant main effects of age and gender on RDDT ear advantages, but no significant interaction between them. Posthoc tests with Bonferroni correction revealed that the main effect of age for the RDDT occurred between 5-year-old children and children at 6, 7, 8, and 10 years of age and between 7-year-old children and children 11 and 12 years of age. Males produced a higher average ear advantage on the RDDT also (see Fig. 1) and children at age 5 produced an average LEA. The main effects of age on RDDT results may have been due to fewer children at the youngest ages. Children between ages 5 and 7 represented the smallest group studied with the RDDT (21% of the total) and among them were 4 left-handed children, compared to 2 left-handers among the children ages 8–10 years (32% of the total) and 6 among the children 11–12 years (47% of the total). More children between the ages of 5 and 7 (33% of the total) were represented in the DWT results for which there was no effect of age. It is possible that a higher proportion of 5-year-old left-handed children led to a strong average LEA when tested with the RDDT. At age 7, the significant differences in RDDT results appear to be due to a dramatic shift toward a larger REA. That age group was also smaller, suggesting that a large effect could have been influenced by relatively few subjects. An REA greater than 40% was demonstrated
Table 2 Top panel: main effects and interactions from a univariate ANOVA on RDDT and DWT ear advantages. Bottom panel: main effects and interactions from a repeated measures ANOVA on method used to calculate RDDT and DWT ear advantages (DL = dichotic listening). DL test
*
df
Error
Univariate analysis of variance on main effects and interactions with ear advantages RDDT Ear advantage Age Gender Age gender DWT Ear advantage Age Gender Age gender
7 1 7 7 1 7
246 246 246 240 240 240
5.328 3.942 1.541 0.638 4.951 1.096
<.001* .048* .154ns .724ns .027* .367ns
Repeated measures ANOVA on methods of calculating ear advantages RDDT Method Method age group Age group DWT Method Gender Age group
1 2 2 1 1 2
241 241 241 235 235 235
20.577 7.604 16.866 31.548 5.381 4.385
<.001* .001* <.001* <.001* .021* .014*
Significant findings.
Within-Ss
Between-Ss
F
p
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
Fig. 1. Mean ear advantages for males and females when tested with the DWT and RDDT are shown with standard error bars. Males produced significantly higher ear advantages than females with the DWT.
by 4 of the 11 males and 3 of the 15 females which may have shifted the ear advantage magnitude higher among those children. To further explore the relationship between ear advantage category and stimulus type (digits versus words), the frequency of each ear advantage type was analyzed by cross tabulation of data for only those children who were tested with both the DWT and the RDDT on the same date (n = 160). Handedness was known for all of these children and there were 3 left-handed females (out of 82) and 6 left-handed males (out of 78). To counteract the effects of fewer children at age 5, age groups were created for these analyses. Pearson Chi-square results revealed that ear advantage frequencies differed between the DWT and RDDT among children in the 8 to 10 years group, v2 (2, 100) = 7.934, p = .019, and in the 11 to 12 years group, v2 (2, 132) = 11.590, p = .003. As shown in Fig. 2A, these results appear to be more heavily influenced by the frequencies of the LEA which differed between the two types of stimuli within those age groups. Results for younger children, however, were more strongly associated. A possible explanation for greater differences in frequencies of each ear advantage type between the two tests is that a greater number of the older children produced equal performance in both ears with the RDDT, leading
319
Fig. 3. Prevalence of no ear advantage (NEA) is shown for children within each age group when tested with the DWT and the RDDT. Older children produced a high prevalence of NEA when tested with the RDDT.
to the NEA. More NEA results reduce REA and/or LEA prevalence. There was a dramatic rise in NEA prevalence among the oldest group of children from 10% to nearly 23% when tested with the RDDT whereas NEA prevalence for the DWT remained low across all age groups (see Fig. 3). Because of the significant effects of gender on ear advantage scores, the same cross tabulations were performed separately for male and female subjects. Significant differences in frequency of ear advantage direction occurred among females tested with DWT, v2 (4, 82) = 12.042, p = .017. The differences were most significant among 8- to 10-year-old females, v2 (2, 50) = 6.000 (df = 2), p = .050. As shown in Fig. 4A, this effect appears to be due to a higher LEA prevalence with the DWT than with the RDDT. Significant test-related differences also occurred among 11- to 12year-old males, v2 (2, 58) = 10.088, p = .006 who also produced a higher LEA prevalence with the DWT. LEA prevalence with dichotic words rose to a surprising 37.9% for males in the oldest age group. There were two left-handed males in that age group and only one of them produced a LEA on the DWT. REA prevalence among male and female children tested with both tests is displayed in Fig. 4B. Average REA prevalence with the DWT ranged from 40% among the youngest females to over 80% among the males in the middle age group. Across all of the children in this subset (n = 160), REA
Fig. 2. Prevalence of leftward (LEA) and rightward (REA) ear advantages are shown within each of the 3 age groups tested. In (A), LEA prevalence decreased in a linear manner with age when children were tested with digits (gray bars), but remained more stable when children were tested with words (black bars). In (B), REA prevalence demonstrated no age-related trend for either digits (gray bars) or words (black bars).
320
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
Fig. 4. Prevalence of leftward (LEA) and rightward (REA) ear advantages are shown separately for males and females within each of the 3 age groups tested. In (A), LEA prevalence increased with age among males and decreased with age among females tested with the DWT but showed a similar decrease with age when both males and females were tested with the RDDT. In (B), REA prevalence varied across test type and gender.
prevalence was 73.8% with the RDDT and 67.6% with the DWT. These results were compared to REA prevalence across all of the children in the study which were similar at 75% with the RDDT (n = 247) and 70% with the DWT (n = 241). 4. Degree of ear advantage Ear advantages were calculated for all children in the study in the traditional manner by subtracting the score for the left ear from the score for the right ear. They were also calculated in the alternative manner by subtracting the score for the non-dominant ear (the lower score) from the score for the dominant ear. The two methods for calculating ear advantage were compared by repeated measures ANOVA and there were significant main effects of calculation method and age group with both tests as shown in Table 2. There were significant main effects of gender on methods of calculating DWT ear advantages when results for both methods were combined (average for males = 13.3%, average for females = 9.5%). There was also a significant interaction between calculation method and age group with the RDDT. As predicted, the traditional method for calculating ear advantage that incorporates negative values for children demonstrating an LEA produced a significantly smaller value for results from both tests than the value calculated by the alternative method (see Fig. 5). Average ear advantages were larger among younger children with both tests, regardless of the method used to calculate them. Post-hoc comparisons using the Dunnett t-test which treated the oldest age group as a control indicated significant differences between all age groups for DWT results (p = .014 for comparison to the youngest age group and p = .049 for comparison to the middle age group). Significant differences between all age groups were also noted for RDDT results (p < .001 for comparison to the youngest age group and p = .001 for comparison to the middle age group). An age-related trend toward smaller ear advantages was stronger in alternative method results than in averages calculated traditionally (see Fig. 6). The traditional method suggested a reduction in average ear advantage of approximately 3% for DWT (Fig. 6B) and 9% for RDDT (Fig. 6A) as children matured from age 5 to age 12. When calculated without regard to right or left ear, the average age-related downward shift of interaural asymmetry was 8% for DWT and 19% for RDDT. With both digits and words, the alternative method for calculating ear advantage revealed an age-related decrease in average ear advantage values that was more than double the size of the change observed with the traditional method.
Fig. 5. Compared to the traditional method of determining ear advantage by subtracting the score for the left ear from the score for the right ear (shown by the broken line), the alternative method that that determines ear advantage by subtracting the lower score from the higher score without regard to which ear was superior (shown by the solid line) demonstrates a significantly larger average ear advantage value for results from both the DWT and the RDDT. Standard error bars are shown.
5. Summary and conclusions The fact that a majority of children produced the REA across both of these tests is not surprising, especially among those who were right-handed. The prevalence of the LEA, however, occurred at a higher prevalence than expected from previous literature. The distribution of RDDT ear advantages in this study neared the REA rates of 80–85% and LEA or NEA rates of 15–20% among right-handed adults and 10- to 18-year-old children previously reported with the RDDT (Moncrieff & Wilson, 2009). These results are also similar to REA rates reported from a study of adults performing the Fused Dichotic Words Test (Hiscock et al., 2005). With the DWT, a lower REA prevalence occurred among both left- and right-handed children, with roughly one-quarter of them demonstrating the LEA across all 3 age groups. Males in the oldest age group produced the largest LEA prevalence. All of the oldest age group males and all of the youngest age group females who produced the LEA with dichotic words were recruited to participate in the normative study. None of them had been referred for
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
321
Fig. 6. Age-related trends toward lower ear advantage values calculated according to the alternative method are shown. In (A), the contrast between the two methods is significant for the youngest and oldest age groups of children tested with digits (RDDT). In (B), the contrast between the two methods is significant across all age groups for children tested with words (DWT). Standard error bars are shown.
a clinical auditory processing assessment. Single-syllable words are thought to involve the highest verbal workload for dichotic testing, so it would be expected that a dichotic words test would be optimal for reflecting hemispheric dominance for language. If that is the case, then results from this study would suggest that more children than expected may have right hemispheric dominance for language as reflected by evidence of stronger performance in their left ears. Prevalence of each ear advantage was markedly different between the two tests used in this study. If more children were right hemisphere dominant for language, LEA prevalence should also have been higher than expected when the same children were tested with the RDDT, but it was not. It is possible that the higher NEA prevalence seen in the oldest age group with dichotic digits may have reduced their LEA prevalence, but it could equally have reduced the REA prevalence. Because digits represent a closed set of highly learned verbal stimuli, they may fail to engage the language-dominant hemisphere as effectively as single syllable words and thereby lower the relative advantage in the contralateral ear so that no ear advantage results, especially among older children whose verbal working memory skills are likely to be more developed. Trends toward a more prevalent REA with increasing age led to theories that hemispheric lateralization stabilizes as children mature and experience language (Asbjørnsen & Helland, 2006; Kershner & Morton, 1990). Other researchers reported that the REA remained constant across age (Berlin et al., 1973; Bryden & Allard, 1981; Morris et al., 1984). LEA prevalence with dichotic words remained stable at approximately 25% across the 3 age groups but there was a significant confound of gender in these results. With age, REA prevalence increased among females and decreased among males. This suggests that there may be a greater influence of gender on dichotic listening with single syllable words than previously thought which does not appear to have the same impact on dichotic listening with digits. The increase in NEA prevalence with digits may have also lowered REA or LEA prevalence among the oldest group of children. The 2-pairs condition of the RDDT draws more heavily on verbal working memory resources because during presentation of the 2 pairs, the listener is uncertain if a third pair will be presented (Strouse & Wilson, 1999). That circumstance may tax working memory more for younger children and lead to larger ear differences. Weaknesses in verbal working memory may have contributed to the instability of ear advantages observed with RDDT testing among the youngest children in the study. By age 7, improvements in working memory may have led to stronger,
balanced performance in the two ears for this closed set of highly familiar stimuli. Results from this study are consistent with reports that younger children produce larger ear advantages whether tested with digits or words, especially when the magnitude of the ear advantage is calculated without regard to its direction toward the right or left ear. It is possible that a larger ear advantage is a more distinguishing characteristic of immature dichotic listening skills than its rightward or leftward direction. Weaknesses in attention or verbal working memory can reduce performance during dichotic listening tasks in ways that may be highly variable among younger children. A structural explanation for a larger ear advantage is that transmission of auditory information from the non-dominant ear to the language dominant ipsilateral hemisphere via the corpus callosum may be weak or compromised (Morton, 1994; Swanson & Cochran, 1991), possibly due to less myelination in the immature brain. Another possible factor for weakness in the non-dominant ear is greater suppression from the dominant ear, like the suppression reported in the visual system in individuals with amblyopia or ‘‘lazy eye.’’ This could lead to a similar auditory dysfunction characterized by normal performance in the child’s dominant ear together with significantly reduced performance in the nondominant or ‘‘lazy’’ ear, thereby producing a larger than normal ear advantage. This auditory disorder has been termed ‘‘amblyaudia’’ (Moncrieff, 2010). A recent study that reported disrupted auditory patterning from suppression by the open ear following surgically induced unilateral conductive hearing loss in rats referred to this phenomenon as ‘‘amblyaudio’’ (Popescu & Polley, 2010). The large ear advantage in some children with amblyaudia has been reduced with treatment, suggesting that interaural asymmetries during dichotic listening can be modified with specific auditory training (Moncrieff & Wertz, 2008). Age-related reductions in ear advantage in this study together with effects of training on lowering abnormally high ear advantages suggest that smaller differences between the two ears during dichotic listening tests may be a hallmark of maturity and enhanced auditory processing. Normative data for degrees and directions of ear advantages during dichotic tasks among younger children could improve clinical diagnosis of auditory processing weaknesses in this vulnerable population that is currently underserved by clinical audiologists and lead to earlier interventions. Results from this study do not fully resolve the question of whether direction of ear advantage is innate or modifiable with experience. It appears that the answer may depend upon the nature of the dichotic stimulus and the gender of the listener. Results from this
322
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
study do demonstrate that despite the variability of results and the interactions of gender and handedness seen with digits testing, children below the age of 7 years can perform these dichotic listening tests and that normative data from children within this youngest age group can and should be measured. They also suggest that normative information about ear advantage without regard to left and right directions may prove more useful for purposes of clinical diagnosis and intervention in this population. References Annett, M. (1970). Classification of hand preference by association analysis. British Journal of Psychology, 61, 303–321. Asbjørnsen, A. E., & Helland, T. (2006). Dichotic listening performance predicts language comprehension. Laterality, 11(3), 251–262. Berlin, C. I., Hughes, L. F., Lowe-Bell, S. S., & Berlin, H. L. (1973). Dichotic right ear advantage in children 5 to 13. Cortex, 9, 394–401. Broadbent, D. E. (1954). The role of auditory localization in attention and memory span. Journal of Experimental Psychology, 47, 191–196. Bryden, M. P. (1970). Laterality effects in dichotic listening: Relations with handedness and reading ability in children. Neuropsychologia, 8, 443–450. Bryden, M. P., & Allard, F. A. (1981). Do auditory perceptual asymmetries develop? Cortex, 17, 313–318. Fennell, E. B., Satz, P., & Morris, R. (1983). The development of handedness and dichotic listening asymmetries in relation to school achievement: a longitudinal study. Journal of Experimental Child Psychology, 35(2), 248–262. Geffen, G. (1976). Development of hemispheric specialization for speech perception. Cortex, 12, 337–346. Goodglass, H., & Qtjadfasel, F. A. (1954). Language laterality in left-handed aphasics. Brain, 77, 521–548. Helland, T., & Asbjornsen, A. (2001). Brain asymmetry for language in dyslexic children. Laterality, 6(4), 289–301. Hiscock, M., Inch, R., & Ewing, C. T. (2005). Constant and variable aspects of the dichotic listening right-ear advantage: A comparison of standard and signal detection tasks. Laterality, 10(6), 517–534. Katz, J., Basil, R. A., & Smith, J. M. (1963). A staggered spondaic word test for detecting central auditory lesions. Annals of Otology, Rhinology and Laryngology, 72,908–917. Kershner, J. R., & Morton, L. L. (1990). Directed attention dichotic listening in reading disabled children: a test of four models of maladaptive lateralization. Neuropsychologia, 28(2), 181–198. Kimura, D. (1961). Cerebral dominance and the perception of verbal stimuli. Canadian Journal of Psychology, 15, 166–171. Kimura, D. (1963). Speech lateralization in young children as determined by an auditory test. Journal of Comparative Physiology and Psychology, 56, 899–902.
Larsen, S. (1984). Developmental changes in the pattern of ear asymmetry as revealed by a dichotic listening task. Cortex, 20(1), 5–17. Martínez, J. A., & Sánchez, E. (1995). Dichotic listening CV lateralization and developmental dyslexia. Journal of Clinical and Experimental Neuropsychology, 21(4), 519–534. Moncrieff, D. W. (2004). Identification of binaural integration deficits in children with the Competing Words Subtest: standard score versus interaural asymmetry. International Journal of Audiology, 45(9), 546–558. Moncrieff, D. W. (2010). Amblyaudia: Evidence of indistinct processing of auditory information in children. Presentation at the American Auditory Society annual meeting, Scottsdale, AZ, March. Moncrieff, D. W., & Black, J. R. (2008). Dichotic listening deficits in children with dyslexia. Dyslexia, 14(1), 54–75. Moncrieff, D. W., & Musiek, F. E. (2002). Interaural asymmetries revealed by dichotic listening tests in normal and dyslexic children. Journal of the American Academy of Audiology, 13(8), 428–437. Moncrieff, D. W., & Wertz, D. (2008). Auditory rehabilitation for interaural asymmetry: preliminary evidence of improved dichotic listening performance following intensive training. International Journal of Audiology, 47(2), 84–97. Moncrieff, D. W., & Wilson, R. H. (2009). Recognition of randomly presented one-, two-, and three-pair dichotic digits by children and young adults. Journal of the American Academy of Audiology, 20, 58–70. Morris, R., Bakker, D., Satz, P., & van der Vlugt, H. (1984). Dichotic listening ear asymmetry: patterns of longitudinal development. Brain and Language, 22(1), 49–66. Morton, L. L. (1994). Interhemispheric balance patterns detected by selective phonemic dichotic laterality measures in four clinical subtypes of readingdisabled children. Journal of Clinical and Experimental Neuropsychology, 16(4), 556–567. Morton, L. L., & Siegel, L. S. (1991). Left ear dichotic listening performance on consonant-vowel combinations and digits in subtypes of reading-disabled children. Brain and Language, 40(2), 162–180. Musiek, F. E. (1983). Assessment of central auditory dysfunction: The dichotic digit test revisited. Ear and Hearing, 4(2), 79–83. Neijenhuis, K., Snik, A., & van den Broek, P. (2003). Auditory processing disorders in adults and children: evaluation of a test battery. International Journal of Audiology, 42(7), 391–400. Obrzut, J. E., Conrad, P. F., & Boliek, C. A. (1989). Verbal and nonverbal auditory processing among left- and right-handed good readers and reading-disabled children. Neuropsychologia, 27(11–12), 1357–1371. Popescu, M. V., & Polley, D. B. (2010). deprivation disrupts development of binaural selectivity in auditory midbrain and cortex. Neuron, 65(5), 718–731. Strouse, A., & Wilson, R. H. (1999). Stimulus length uncertainty with dichotic digit recognition. Journal of the American Academy of Audiology, 10(4), 219–229. Swanson, H. L., & Cochran, K. F. (1991). Learning disabilities, distinctive encoding, and hemispheric resources. Brain and Language, 40(2), 202–230.
Contents lists available at ScienceDirect
Brain and Cognition journal homepage: www.elsevier.com/locate/b&c
Dichotic listening in children: Age-related changes in direction and magnitude of ear advantage Deborah W. Moncrieff ⇑ University of Pittsburgh, 4033 Forbes Tower, Pittsburgh, PA 15260, United States
a r t i c l e
i n f o
Article history: Available online 6 May 2011 Keywords: Dichotic Ear advantage Lateralization Development Children Amblyaudia
a b s t r a c t Children between the ages of 5 and 12 years were tested with dichotic listening tests utilizing single syllable words and random presentations of digits. They produced a higher prevalence of left ear dominance than expected, especially among right-handed children when tested with words. Whether more children demonstrate the LEA because of right hemisphere dominance for language or because there is less stability in ear advantage direction at younger ages cannot be fully resolved by this study. When ear advantages were measured by subtracting each child’s lower score from the higher score without regard to right or left direction, an age-related trend toward lower measures of ear advantage was evident. This trend was greater for dichotic words than for dichotic digits. Structural factors that may be related to these results and possible influences of attention and verbal workload on the two kinds of dichotic stimuli are discussed. Ó 2011 Elsevier Inc. All rights reserved.
1. Introduction We measure hearing one ear at a time, but listening occurs through both ears and complete parity of signals arriving at the right and left ear at any given time is relatively rare. Therefore, the intake of information through the auditory system requires an online integration of differing and potentially competing information presented to the two ears. Broadbent (1954) first reported that when two different words were presented to the right and left ear simultaneously, normal listeners could accurately identify more words heard at their right ear. Later, Doreen Kimura (1961) ascribed the dichotic listening right ear advantage (REA) to stronger crossed auditory pathways from the right ear ascending directly to the speech-dominant left cerebral hemisphere. She further noted that the REA was enhanced by suppression of information ascending via the ipsilateral pathway from the left ear to the speech-dominant left hemisphere. At the time, researchers were concerned that handedness may not be an accurate index of hemispheric dominance for language (Goodglass & Otjadfasel, 1954) and they saw the dichotic listening ear advantage as a potentially better method for determining lateralization. Shortly after her groundbreaking study of dichotic listening in adults, Kimura (1963) reported that right-handed children from age 4 to 9 years produced an average REA, suggesting a contralateral left hemisphere lateralization for speech stimuli as early as age 4 years or before. She also noted that cerebral dominance
⇑ Fax: +1 412 383 6555. E-mail address: [email protected] 0278-2626/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2011.03.013
may not be rigidly established in younger children, beginning a controversy over development of ear advantage and language lateralization that persists today. Bryden (1970) reported that the prevalence of an REA increased from 2nd to 6th grade among right-handers, suggesting that left hemisphere dominance for language may not be firmly established in younger children. He also reported that some left-handers switched to a left-ear advantage (LEA) by the 6th grade, raising the possibility that direction of ear advantage is subject to developmental factors and that right hemisphere dominance may also be normal. Some reported that the magnitude of the REA changed with age as children became more strongly lateralized for language (Fennell, Satz, & Morris, 1983) but others reported that the REA remained the same when tested with consonant–vowels (CVs) (Berlin, Hughes, Lowe-Bell, & Berlin, 1973), words (Geffen, 1976), or CVs, words, and digits (Bryden & Allard, 1981). A statistical analysis of two longitudinal studies utilizing dichotic digits in school-age subjects found no developmental pattern and concluded that dichotic listening in the free recall mode may be ineffective for measuring lateralization (Morris, Bakker, & Satz, 1984). This prompted a flurry of research into response techniques to add control over the listener’s attention, but these also failed to produce a reliable pattern of development. For many decades, researchers interested in development of cerebral dominance and its impact on language and learning have used the dichotic listening technique to investigate these issues. With digits, words, and CVs, they have compared free recall and directed response methodologies, and have asked children to respond by recognition, memory, or repetition techniques. Some have reported a larger REA in children with disabilities when
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
tested with digits and words because of lower reports of stimuli from the left ear (Kershner & Morton, 1990; Moncrieff & Black, 2008; Morton & Siegel, 1991) whereas others reported a weaker REA or the LEA when children with disabilities were tested with CVs (Helland & Asbjornsen, 2001; Martínez & Sánchez, 1995; Moncrieff & Black, 2008; Morton & Siegel, 1991; Obrzut, Conrad, & Boliek, 1989). Some dichotic listening tests with words and digits have been administered to children from age 5 to age 18 for the purpose of establishing normative data so that the tests can be administered clinically. Normative information is available as separate right and left ear scores and test results are compared to standard values to determine if one or both ears fall below normal (Katz, Basil, & Smith, 1963; Moncrieff & Wilson, 2009; Musiek, 1983). Average values of the REA and the overall prevalence of the LEA at each age level in normative studies are typically not reported, but there does appear to be a decrease in magnitude of the REA when children are tested with digits and words, but not when they are assessed with CVs. A recent study compared the incidence of abnormal results when magnitude of the REA was used instead of standard scoring techniques and reported that ear advantage magnitude may be more effective at determining clinically significant results than individual or combined ear scores when assessing children’s dichotic listening (Moncrieff, 2004). Additional information about direction and magnitude of ear advantage could reveal age-related trends in development of dichotic listening skills. Normative values for ear advantage based on the absolute difference between the two ears without regard to right or left might be more useful in determining clinically significant outcomes in children. Current normative data fails to account for inclusion of left-ear dominance among children tested. Therefore, a true measure of ear advantage at each age could be underestimated. Long ago, Larsen (1984) suggested that stable ear advantage values in young children may be due to the customary practice of determining them by subtracting the left ear score from the right ear score. If younger children produce larger ear advantages and several produce the LEA, the presence of LEA data yields negative values that when added to the positive values for REAs would yield lower averages across children within that age group. Larsen reported that when differences between the two ears were calculated for each individual child, developmental patterns emerged. Similarly, absolute values for ear differences could provide important evidence of how the magnitude of ear advantage changes with development. Information about age-related prevalence of the LEA would also address whether direction of ear advantage changes with maturity, with some children switching from LEA to REA. A consistent REA prevalence, similar to the reported 80–85% of right-handed adults and 50% of left-handed adults (Hiscock, Inch, & Ewing, 2005), would support the notion that hemispheric dominance is fully lateralized at birth. In contrast, if ear advantage direction depends on developmental factors, then REA prevalence could increase or decrease as children mature. Bryden’s (1970) report of a higher prevalence of the LEA among younger children suggested that direction of ear advantage may be unstable among younger children and that some switch from the LEA to the REA as a consequence of normal development. Two new dichotic listening tests have been developed and normative information is currently being gathered from school-age children. A preliminary review of results from this data collection will be reported here to explore whether direction and degree of ear advantage are stable across school-age development. Stability of ear advantage direction will be confirmed if the prevalence of the REA and the LEA remains similar across all age levels. Increases in prevalence of either the REA or LEA would support the notion
317
that developmental increases in attention, working memory and/ or language skills affect ear advantage direction. Finally, because the magnitude of ear advantage may be underestimated at each age level by numerically averaging across children with both REAs and LEAs, ear advantages will also be calculated as the numerical difference between the dominant and non-dominant ear without regard to right or left. Age-related changes in ear advantage using both the traditional method and this alternative method will be examined for developmental trends and the two methods will be compared for significant differences.
2. Methods Children ages 5–12 years participated in the study. Most were recruited for a normative study and others were assessed as part of a clinical evaluation for auditory processing (23 of the 50 children evaluated clinically were thought to have greater than normal difficulty with dichotic listening). Results from both classes of children are included in this study because it is not intended as a normative sample per se but is interested in magnitude and direction of ear advantage within individual age groups. Each child participated with the consent of a parent or legal guardian in accordance with policies of the university institutional review board or the clinical site at which they were assessed. Children were tested at various locations, including a quiet room at their school or home, at a hospital, at a clinical practice, or at a university research laboratory. All children had normal hearing with no pure tone thresholds poorer than 20 dB HL in either ear at the time of testing. Handedness was assessed by a modified survey which asked about use of everyday items such as a toothbrush, pen for writing a letter, or scissors (Annett, 1970). In some cases, handedness was not assessed. Two different dichotic listening tests were used. Normative data for one of the tests, the Randomized Dichotic Digits Test (RDDT), has been previously reported for children ages 10 to 18 years (Moncrieff & Wilson, 2009). The RDDT lacks the ceiling effects that have been found among older children when tested with double dichotic digits (Moncrieff & Musiek, 2002; Neijenhuis, Snik, & van den Broek, 2003). The Dichotic Words Test (DWT) is a new dichotic listening test comprised of single syllable words. Stimuli for the DWT were created by aligning two single syllable words spoken in a male voice, each matched for time of onset and time of offset so that the total duration of each word in a pair was identical. Four lists of 25 words were created so that each list was balanced for phonemic content. The initial and final consonant and medial vowel were balanced to the extent possible within each list and across the four lists. Average root mean square (RMS) amplitude was equalized for each word so that all stimuli were presented at the same RMS amplitude across the entire test. Digits and words were presented at a comfortable listening level to the two ears, either at 50 dB HL bilaterally through insert earphones or TDH-50 supra-aural earphones attached to a clinical audiometer or through Sennheiser 280 Pro circumaural earphones attached to a Dell laptop computer with output level confirmed by the examiner prior to beginning the test. Each time, the intensity was balanced across the two ears so that the presentation to the right ear was always at the same intensity as the presentation to the left ear. Children were instructed to listen for the digits or words and to repeat everything that they had heard from each ear. All children completed two word lists and the randomized list of digits in a free recall paradigm in which they were given no specific instructions about the order for reporting what they heard. A subset of children also completed two other lists of the DWT in a directed response format during which they were instructed to repeat the word heard in their right ear first for one list and the word heard in their left ear first for another list. The number of correct
318
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
responses was converted to percentage for the 1-pair, 2-pairs and 3-pairs conditions of the RDDT and across each list of the DWT. DWT lists were chosen randomly from among the four lists available for each child tested. Ear advantages were measured two ways. In the first traditional way, the score for the left ear was subtracted from the score for the right ear which yields a positive number for a REA, a negative number for a LEA, and zero for no ear advantage (NEA). Results were used to measure the prevalence of ear advantage directions and to produce an average value among children in each age group. In the second case, the lower score was subtracted from the higher score to yield an ear advantage that provides the difference between the child’s dominant and non-dominant ears without regard to right or left. Again, an average value for ear advantage was measured for the children within each age group. The two average values for ear advantage were compared for significant differences. 3. Results A total of 247 children were tested with the RDDT and 241 children were tested with the DWT in the free recall format. Among
Table 1 Demographics regarding the number of male and female children at each age level included in the study and indicating their handedness if known. Age
Males L-Hand
Females R-Hand
Total
Unknown
L-Hand
R-Hand
Unknown
1 2 1 2 5 4 4 3 22
1 1 1 0 1 0 1 0 5
5 10 19 11 11 8 22 15 101
0 1 5 4 1 1 3 2 17
14 26 39 35 28 20 49 30 241
Randomized dichotic digits test 5 1 4 0 6 1 8 1 7 1 9 1 8 1 14 2 9 0 6 3 10 0 11 7 11 4 25 9 12 0 17 4 Total 8 94 27
0 1 0 0 1 0 1 1 4
4 7 9 10 7 12 27 20 96
0 0 5 4 1 1 5 2 18
9 18 25 31 18 31 71 44 247
Dichotic words test 5 1 6 6 1 11 7 1 12 8 1 17 9 1 9 10 0 7 11 2 17 12 0 10 Total 7 89
those tested with the DWT, some were also tested in the directed response format (n = 145). A paired t-test on DWT ear advantages between the free recall and directed response formats among those who were tested both ways showed no significant differences in ear advantages, t = .586, p = .559, so scores for the two free recall lists of the DWT were used for determining ear advantages in this study. Another paired t-test on differences in RDDT ear advantages between the 2-pairs condition and the overall test also failed to achieve significance, t = 1.905, p = .058, so scores for the 2-pairs condition of the RDDT were used. Demographics regarding age, gender, and handedness of children involved in the study are shown in Table 1. A total of 190 children tested with the RDDT were right-handed (96 females and 94 males) and similarly, 190 of the children tested with the DWT were right-handed (89 females and 101 males). Ear advantages were compared between right-handed children and all other children in the study (left-handed and handedness unknown) by univariate analysis of variance (ANOVA) and no significant differences in ear advantages were noted for the RDDT, F(1, 246) = 1.902, p = .169, or the DWT, F(1, 240) = 1.370, p = .243. As shown in Table 2, the only significant main effect on ear advantage when children were tested with the DWT occurred for gender because the average overall REA was greater among males than females (see Fig. 1). Age failed to produce any significant effects on DWT ear advantages. There were significant main effects of age and gender on RDDT ear advantages, but no significant interaction between them. Posthoc tests with Bonferroni correction revealed that the main effect of age for the RDDT occurred between 5-year-old children and children at 6, 7, 8, and 10 years of age and between 7-year-old children and children 11 and 12 years of age. Males produced a higher average ear advantage on the RDDT also (see Fig. 1) and children at age 5 produced an average LEA. The main effects of age on RDDT results may have been due to fewer children at the youngest ages. Children between ages 5 and 7 represented the smallest group studied with the RDDT (21% of the total) and among them were 4 left-handed children, compared to 2 left-handers among the children ages 8–10 years (32% of the total) and 6 among the children 11–12 years (47% of the total). More children between the ages of 5 and 7 (33% of the total) were represented in the DWT results for which there was no effect of age. It is possible that a higher proportion of 5-year-old left-handed children led to a strong average LEA when tested with the RDDT. At age 7, the significant differences in RDDT results appear to be due to a dramatic shift toward a larger REA. That age group was also smaller, suggesting that a large effect could have been influenced by relatively few subjects. An REA greater than 40% was demonstrated
Table 2 Top panel: main effects and interactions from a univariate ANOVA on RDDT and DWT ear advantages. Bottom panel: main effects and interactions from a repeated measures ANOVA on method used to calculate RDDT and DWT ear advantages (DL = dichotic listening). DL test
*
df
Error
Univariate analysis of variance on main effects and interactions with ear advantages RDDT Ear advantage Age Gender Age gender DWT Ear advantage Age Gender Age gender
7 1 7 7 1 7
246 246 246 240 240 240
5.328 3.942 1.541 0.638 4.951 1.096
<.001* .048* .154ns .724ns .027* .367ns
Repeated measures ANOVA on methods of calculating ear advantages RDDT Method Method age group Age group DWT Method Gender Age group
1 2 2 1 1 2
241 241 241 235 235 235
20.577 7.604 16.866 31.548 5.381 4.385
<.001* .001* <.001* <.001* .021* .014*
Significant findings.
Within-Ss
Between-Ss
F
p
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
Fig. 1. Mean ear advantages for males and females when tested with the DWT and RDDT are shown with standard error bars. Males produced significantly higher ear advantages than females with the DWT.
by 4 of the 11 males and 3 of the 15 females which may have shifted the ear advantage magnitude higher among those children. To further explore the relationship between ear advantage category and stimulus type (digits versus words), the frequency of each ear advantage type was analyzed by cross tabulation of data for only those children who were tested with both the DWT and the RDDT on the same date (n = 160). Handedness was known for all of these children and there were 3 left-handed females (out of 82) and 6 left-handed males (out of 78). To counteract the effects of fewer children at age 5, age groups were created for these analyses. Pearson Chi-square results revealed that ear advantage frequencies differed between the DWT and RDDT among children in the 8 to 10 years group, v2 (2, 100) = 7.934, p = .019, and in the 11 to 12 years group, v2 (2, 132) = 11.590, p = .003. As shown in Fig. 2A, these results appear to be more heavily influenced by the frequencies of the LEA which differed between the two types of stimuli within those age groups. Results for younger children, however, were more strongly associated. A possible explanation for greater differences in frequencies of each ear advantage type between the two tests is that a greater number of the older children produced equal performance in both ears with the RDDT, leading
319
Fig. 3. Prevalence of no ear advantage (NEA) is shown for children within each age group when tested with the DWT and the RDDT. Older children produced a high prevalence of NEA when tested with the RDDT.
to the NEA. More NEA results reduce REA and/or LEA prevalence. There was a dramatic rise in NEA prevalence among the oldest group of children from 10% to nearly 23% when tested with the RDDT whereas NEA prevalence for the DWT remained low across all age groups (see Fig. 3). Because of the significant effects of gender on ear advantage scores, the same cross tabulations were performed separately for male and female subjects. Significant differences in frequency of ear advantage direction occurred among females tested with DWT, v2 (4, 82) = 12.042, p = .017. The differences were most significant among 8- to 10-year-old females, v2 (2, 50) = 6.000 (df = 2), p = .050. As shown in Fig. 4A, this effect appears to be due to a higher LEA prevalence with the DWT than with the RDDT. Significant test-related differences also occurred among 11- to 12year-old males, v2 (2, 58) = 10.088, p = .006 who also produced a higher LEA prevalence with the DWT. LEA prevalence with dichotic words rose to a surprising 37.9% for males in the oldest age group. There were two left-handed males in that age group and only one of them produced a LEA on the DWT. REA prevalence among male and female children tested with both tests is displayed in Fig. 4B. Average REA prevalence with the DWT ranged from 40% among the youngest females to over 80% among the males in the middle age group. Across all of the children in this subset (n = 160), REA
Fig. 2. Prevalence of leftward (LEA) and rightward (REA) ear advantages are shown within each of the 3 age groups tested. In (A), LEA prevalence decreased in a linear manner with age when children were tested with digits (gray bars), but remained more stable when children were tested with words (black bars). In (B), REA prevalence demonstrated no age-related trend for either digits (gray bars) or words (black bars).
320
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
Fig. 4. Prevalence of leftward (LEA) and rightward (REA) ear advantages are shown separately for males and females within each of the 3 age groups tested. In (A), LEA prevalence increased with age among males and decreased with age among females tested with the DWT but showed a similar decrease with age when both males and females were tested with the RDDT. In (B), REA prevalence varied across test type and gender.
prevalence was 73.8% with the RDDT and 67.6% with the DWT. These results were compared to REA prevalence across all of the children in the study which were similar at 75% with the RDDT (n = 247) and 70% with the DWT (n = 241). 4. Degree of ear advantage Ear advantages were calculated for all children in the study in the traditional manner by subtracting the score for the left ear from the score for the right ear. They were also calculated in the alternative manner by subtracting the score for the non-dominant ear (the lower score) from the score for the dominant ear. The two methods for calculating ear advantage were compared by repeated measures ANOVA and there were significant main effects of calculation method and age group with both tests as shown in Table 2. There were significant main effects of gender on methods of calculating DWT ear advantages when results for both methods were combined (average for males = 13.3%, average for females = 9.5%). There was also a significant interaction between calculation method and age group with the RDDT. As predicted, the traditional method for calculating ear advantage that incorporates negative values for children demonstrating an LEA produced a significantly smaller value for results from both tests than the value calculated by the alternative method (see Fig. 5). Average ear advantages were larger among younger children with both tests, regardless of the method used to calculate them. Post-hoc comparisons using the Dunnett t-test which treated the oldest age group as a control indicated significant differences between all age groups for DWT results (p = .014 for comparison to the youngest age group and p = .049 for comparison to the middle age group). Significant differences between all age groups were also noted for RDDT results (p < .001 for comparison to the youngest age group and p = .001 for comparison to the middle age group). An age-related trend toward smaller ear advantages was stronger in alternative method results than in averages calculated traditionally (see Fig. 6). The traditional method suggested a reduction in average ear advantage of approximately 3% for DWT (Fig. 6B) and 9% for RDDT (Fig. 6A) as children matured from age 5 to age 12. When calculated without regard to right or left ear, the average age-related downward shift of interaural asymmetry was 8% for DWT and 19% for RDDT. With both digits and words, the alternative method for calculating ear advantage revealed an age-related decrease in average ear advantage values that was more than double the size of the change observed with the traditional method.
Fig. 5. Compared to the traditional method of determining ear advantage by subtracting the score for the left ear from the score for the right ear (shown by the broken line), the alternative method that that determines ear advantage by subtracting the lower score from the higher score without regard to which ear was superior (shown by the solid line) demonstrates a significantly larger average ear advantage value for results from both the DWT and the RDDT. Standard error bars are shown.
5. Summary and conclusions The fact that a majority of children produced the REA across both of these tests is not surprising, especially among those who were right-handed. The prevalence of the LEA, however, occurred at a higher prevalence than expected from previous literature. The distribution of RDDT ear advantages in this study neared the REA rates of 80–85% and LEA or NEA rates of 15–20% among right-handed adults and 10- to 18-year-old children previously reported with the RDDT (Moncrieff & Wilson, 2009). These results are also similar to REA rates reported from a study of adults performing the Fused Dichotic Words Test (Hiscock et al., 2005). With the DWT, a lower REA prevalence occurred among both left- and right-handed children, with roughly one-quarter of them demonstrating the LEA across all 3 age groups. Males in the oldest age group produced the largest LEA prevalence. All of the oldest age group males and all of the youngest age group females who produced the LEA with dichotic words were recruited to participate in the normative study. None of them had been referred for
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
321
Fig. 6. Age-related trends toward lower ear advantage values calculated according to the alternative method are shown. In (A), the contrast between the two methods is significant for the youngest and oldest age groups of children tested with digits (RDDT). In (B), the contrast between the two methods is significant across all age groups for children tested with words (DWT). Standard error bars are shown.
a clinical auditory processing assessment. Single-syllable words are thought to involve the highest verbal workload for dichotic testing, so it would be expected that a dichotic words test would be optimal for reflecting hemispheric dominance for language. If that is the case, then results from this study would suggest that more children than expected may have right hemispheric dominance for language as reflected by evidence of stronger performance in their left ears. Prevalence of each ear advantage was markedly different between the two tests used in this study. If more children were right hemisphere dominant for language, LEA prevalence should also have been higher than expected when the same children were tested with the RDDT, but it was not. It is possible that the higher NEA prevalence seen in the oldest age group with dichotic digits may have reduced their LEA prevalence, but it could equally have reduced the REA prevalence. Because digits represent a closed set of highly learned verbal stimuli, they may fail to engage the language-dominant hemisphere as effectively as single syllable words and thereby lower the relative advantage in the contralateral ear so that no ear advantage results, especially among older children whose verbal working memory skills are likely to be more developed. Trends toward a more prevalent REA with increasing age led to theories that hemispheric lateralization stabilizes as children mature and experience language (Asbjørnsen & Helland, 2006; Kershner & Morton, 1990). Other researchers reported that the REA remained constant across age (Berlin et al., 1973; Bryden & Allard, 1981; Morris et al., 1984). LEA prevalence with dichotic words remained stable at approximately 25% across the 3 age groups but there was a significant confound of gender in these results. With age, REA prevalence increased among females and decreased among males. This suggests that there may be a greater influence of gender on dichotic listening with single syllable words than previously thought which does not appear to have the same impact on dichotic listening with digits. The increase in NEA prevalence with digits may have also lowered REA or LEA prevalence among the oldest group of children. The 2-pairs condition of the RDDT draws more heavily on verbal working memory resources because during presentation of the 2 pairs, the listener is uncertain if a third pair will be presented (Strouse & Wilson, 1999). That circumstance may tax working memory more for younger children and lead to larger ear differences. Weaknesses in verbal working memory may have contributed to the instability of ear advantages observed with RDDT testing among the youngest children in the study. By age 7, improvements in working memory may have led to stronger,
balanced performance in the two ears for this closed set of highly familiar stimuli. Results from this study are consistent with reports that younger children produce larger ear advantages whether tested with digits or words, especially when the magnitude of the ear advantage is calculated without regard to its direction toward the right or left ear. It is possible that a larger ear advantage is a more distinguishing characteristic of immature dichotic listening skills than its rightward or leftward direction. Weaknesses in attention or verbal working memory can reduce performance during dichotic listening tasks in ways that may be highly variable among younger children. A structural explanation for a larger ear advantage is that transmission of auditory information from the non-dominant ear to the language dominant ipsilateral hemisphere via the corpus callosum may be weak or compromised (Morton, 1994; Swanson & Cochran, 1991), possibly due to less myelination in the immature brain. Another possible factor for weakness in the non-dominant ear is greater suppression from the dominant ear, like the suppression reported in the visual system in individuals with amblyopia or ‘‘lazy eye.’’ This could lead to a similar auditory dysfunction characterized by normal performance in the child’s dominant ear together with significantly reduced performance in the nondominant or ‘‘lazy’’ ear, thereby producing a larger than normal ear advantage. This auditory disorder has been termed ‘‘amblyaudia’’ (Moncrieff, 2010). A recent study that reported disrupted auditory patterning from suppression by the open ear following surgically induced unilateral conductive hearing loss in rats referred to this phenomenon as ‘‘amblyaudio’’ (Popescu & Polley, 2010). The large ear advantage in some children with amblyaudia has been reduced with treatment, suggesting that interaural asymmetries during dichotic listening can be modified with specific auditory training (Moncrieff & Wertz, 2008). Age-related reductions in ear advantage in this study together with effects of training on lowering abnormally high ear advantages suggest that smaller differences between the two ears during dichotic listening tests may be a hallmark of maturity and enhanced auditory processing. Normative data for degrees and directions of ear advantages during dichotic tasks among younger children could improve clinical diagnosis of auditory processing weaknesses in this vulnerable population that is currently underserved by clinical audiologists and lead to earlier interventions. Results from this study do not fully resolve the question of whether direction of ear advantage is innate or modifiable with experience. It appears that the answer may depend upon the nature of the dichotic stimulus and the gender of the listener. Results from this
322
D.W. Moncrieff / Brain and Cognition 76 (2011) 316–322
study do demonstrate that despite the variability of results and the interactions of gender and handedness seen with digits testing, children below the age of 7 years can perform these dichotic listening tests and that normative data from children within this youngest age group can and should be measured. They also suggest that normative information about ear advantage without regard to left and right directions may prove more useful for purposes of clinical diagnosis and intervention in this population. References Annett, M. (1970). Classification of hand preference by association analysis. British Journal of Psychology, 61, 303–321. Asbjørnsen, A. E., & Helland, T. (2006). Dichotic listening performance predicts language comprehension. Laterality, 11(3), 251–262. Berlin, C. I., Hughes, L. F., Lowe-Bell, S. S., & Berlin, H. L. (1973). Dichotic right ear advantage in children 5 to 13. Cortex, 9, 394–401. Broadbent, D. E. (1954). The role of auditory localization in attention and memory span. Journal of Experimental Psychology, 47, 191–196. Bryden, M. P. (1970). Laterality effects in dichotic listening: Relations with handedness and reading ability in children. Neuropsychologia, 8, 443–450. Bryden, M. P., & Allard, F. A. (1981). Do auditory perceptual asymmetries develop? Cortex, 17, 313–318. Fennell, E. B., Satz, P., & Morris, R. (1983). The development of handedness and dichotic listening asymmetries in relation to school achievement: a longitudinal study. Journal of Experimental Child Psychology, 35(2), 248–262. Geffen, G. (1976). Development of hemispheric specialization for speech perception. Cortex, 12, 337–346. Goodglass, H., & Qtjadfasel, F. A. (1954). Language laterality in left-handed aphasics. Brain, 77, 521–548. Helland, T., & Asbjornsen, A. (2001). Brain asymmetry for language in dyslexic children. Laterality, 6(4), 289–301. Hiscock, M., Inch, R., & Ewing, C. T. (2005). Constant and variable aspects of the dichotic listening right-ear advantage: A comparison of standard and signal detection tasks. Laterality, 10(6), 517–534. Katz, J., Basil, R. A., & Smith, J. M. (1963). A staggered spondaic word test for detecting central auditory lesions. Annals of Otology, Rhinology and Laryngology, 72,908–917. Kershner, J. R., & Morton, L. L. (1990). Directed attention dichotic listening in reading disabled children: a test of four models of maladaptive lateralization. Neuropsychologia, 28(2), 181–198. Kimura, D. (1961). Cerebral dominance and the perception of verbal stimuli. Canadian Journal of Psychology, 15, 166–171. Kimura, D. (1963). Speech lateralization in young children as determined by an auditory test. Journal of Comparative Physiology and Psychology, 56, 899–902.
Larsen, S. (1984). Developmental changes in the pattern of ear asymmetry as revealed by a dichotic listening task. Cortex, 20(1), 5–17. Martínez, J. A., & Sánchez, E. (1995). Dichotic listening CV lateralization and developmental dyslexia. Journal of Clinical and Experimental Neuropsychology, 21(4), 519–534. Moncrieff, D. W. (2004). Identification of binaural integration deficits in children with the Competing Words Subtest: standard score versus interaural asymmetry. International Journal of Audiology, 45(9), 546–558. Moncrieff, D. W. (2010). Amblyaudia: Evidence of indistinct processing of auditory information in children. Presentation at the American Auditory Society annual meeting, Scottsdale, AZ, March. Moncrieff, D. W., & Black, J. R. (2008). Dichotic listening deficits in children with dyslexia. Dyslexia, 14(1), 54–75. Moncrieff, D. W., & Musiek, F. E. (2002). Interaural asymmetries revealed by dichotic listening tests in normal and dyslexic children. Journal of the American Academy of Audiology, 13(8), 428–437. Moncrieff, D. W., & Wertz, D. (2008). Auditory rehabilitation for interaural asymmetry: preliminary evidence of improved dichotic listening performance following intensive training. International Journal of Audiology, 47(2), 84–97. Moncrieff, D. W., & Wilson, R. H. (2009). Recognition of randomly presented one-, two-, and three-pair dichotic digits by children and young adults. Journal of the American Academy of Audiology, 20, 58–70. Morris, R., Bakker, D., Satz, P., & van der Vlugt, H. (1984). Dichotic listening ear asymmetry: patterns of longitudinal development. Brain and Language, 22(1), 49–66. Morton, L. L. (1994). Interhemispheric balance patterns detected by selective phonemic dichotic laterality measures in four clinical subtypes of readingdisabled children. Journal of Clinical and Experimental Neuropsychology, 16(4), 556–567. Morton, L. L., & Siegel, L. S. (1991). Left ear dichotic listening performance on consonant-vowel combinations and digits in subtypes of reading-disabled children. Brain and Language, 40(2), 162–180. Musiek, F. E. (1983). Assessment of central auditory dysfunction: The dichotic digit test revisited. Ear and Hearing, 4(2), 79–83. Neijenhuis, K., Snik, A., & van den Broek, P. (2003). Auditory processing disorders in adults and children: evaluation of a test battery. International Journal of Audiology, 42(7), 391–400. Obrzut, J. E., Conrad, P. F., & Boliek, C. A. (1989). Verbal and nonverbal auditory processing among left- and right-handed good readers and reading-disabled children. Neuropsychologia, 27(11–12), 1357–1371. Popescu, M. V., & Polley, D. B. (2010). deprivation disrupts development of binaural selectivity in auditory midbrain and cortex. Neuron, 65(5), 718–731. Strouse, A., & Wilson, R. H. (1999). Stimulus length uncertainty with dichotic digit recognition. Journal of the American Academy of Audiology, 10(4), 219–229. Swanson, H. L., & Cochran, K. F. (1991). Learning disabilities, distinctive encoding, and hemispheric resources. Brain and Language, 40(2), 202–230.