Binaural Masking Release in Children With Down Syndrome Heather L. Porter,1,2 D. Wesley Grantham,1 Daniel H. Ashmead,1 and Anne Marie Tharpe1 Objectives: Binaural hearing results in a number of listening advantages relative to monaural hearing, including enhanced hearing sensitivity and better speech understanding in adverse listening conditions. These advantages are facilitated in part by the ability to detect and use interaural cues within the central auditory system. Binaural hearing for children with Down syndrome could be impacted by multiple factors including, structural anomalies within the peripheral and central auditory system, alterations in synaptic communication, and chronic otitis media with effusion. However, binaural hearing capabilities have not been investigated in these children. This study tested the hypothesis that children with Down syndrome experience less binaural benefit than typically developing peers.

Key words: Binaural hearing, Binaural intelligibility level difference, Down syndrome, Masking level difference. (Ear & Hearing 2014;35;e134–e142)

INTRODUCTION Down syndrome is the most common chromosomal condition, occurring in approximately 1 in 700 births in the United States (Parker et al. 2010). Phenotypic characteristics of Down syndrome include developmental delay, disorders of the endocrine, cardiovascular, and gastrointestinal systems, and multiple issues specific to the auditory system including stenotic ear canals, ossicular malformations, and inner ear dysplasia (for review, see Roizen 2010). In addition, children with Down syndrome are more likely than typically developing children to have chronic otitis media with concomitant hearing loss. Chronic conductive hearing loss has been found to result in delayed development in some aspects of auditory perception (Hall & Grose 1993; Hall et al. 1995). These potential influences on auditory development are compelling reasons to explore the status of auditory perceptual skills in children with Down syndrome. The present study focuses on binaural masking release for pure-tone and speech signals presented in masking noise. Before describing the specific tests used in this study, the hypothetical basis for studying auditory perception in this population will be briefly considered.

Design: Participants included children with Down syndrome aged 6 to 16 years (n = 11), typically developing children aged 3 to 12 years (n = 46), adults with Down syndrome (n = 3), and adults with no known neurological delays (n = 6). Inclusionary criteria included normal to near-normal hearing sensitivity. Two tasks were used to assess binaural ability. Masking level difference (MLD) was calculated by comparing threshold for a 500-Hz pure-tone signal in 300-Hz wide Gaussian noise for N0S0 and N0Sπ signal configurations. Binaural intelligibility level difference was calculated using simulated free-field conditions. Speech recognition threshold was measured for closed-set spondees presented from 0-degree azimuth in speech-shaped noise presented from 0-, 45- and 90-degree azimuth, respectively. The developmental ability of children with Down syndrome was estimated and information regarding history of otitis media was obtained for all child participants via parent survey. Results: Individuals with Down syndrome had higher masked thresholds for pure-tone and speech stimuli than typically developing individuals. Children with Down syndrome had significantly smaller MLDs than typically developing children. Adults with Down syndrome and control adults had similar MLDs. Similarities in simulated spatial release from masking were observed for all groups for the experimental parameters used in this study. No association was observed for any measure of binaural ability and developmental age for children with Down syndrome. Similar group psychometric functions were observed for children with Down syndrome and typically developing children in most instances, suggesting that attentiveness and motivation contributed equally to performance for both groups on most tasks.

Anatomical and Physiological Factors in Children With Down Syndrome A large body of histologic, radiologic, and electrophysiologic evidence describes altered anatomy and synaptic communication within the central auditory system of children with Down syndrome (e.g., Banik et al. 1975; Becker et al. 1986; Pinter et al. 2001; Kittler et al. 2009). Histologic and radiologic evidence shows that individuals with Down syndrome have smaller cortical and subcortical structures compared with individuals without Down syndrome (e.g., Crome et al. 1966; Wisniewski 1990; Pinter et al. 2001). Examination of dendritic branching in the visual cortex indicates atrophy early in childhood for children with Down syndrome (Takashima et al. 1981; Becker et al. 1986). Furthermore, individuals with Down syndrome have reduced myelin in cortical white matter and lower neuronal density in cortical layers II and IV compared with their typically developing peers (Banik et al. 1975; Wisniewski 1990). In addition to resulting in other known neurological implications, the altered neural anatomy for children with Down syndrome raises the possibility that they could process auditory information differently from their typically developing peers. The idea that Down syndrome might be associated with abnormal auditory processing receives some support from electrophysiologic studies. In general, auditory brainstem response

Conclusions: The binaural advantages afforded to typically developing children, such as enhanced hearing sensitivity in noise, were not as robust for children with Down syndrome in this study. Children with Down syndrome experienced less binaural benefit than typically developing peers for some stimuli, suggesting that they could require more favorable signal-to-noise ratios to achieve optimal performance in some adverse listening conditions. The reduced release from masking observed for children with Down syndrome could represent a delay in ability rather than a deficit that persists into adulthood. This could have implications for the planning of interventions for individuals with Down syndrome.

Department of Hearing and Speech Sciences, Vanderbilt University, Nashville, Tennessee, USA; and 2Department Of Otolaryngology—Head and Neck Surgery University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA. 1

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(ABR) latencies are decreased whereas cortical latencies are increased for infants, older children, and adults with Down syndrome compared with their age-matched, typically developing peers (Folsom et al. 1983; Jiang et al. 1990; Seidl et al. 1997; Forti et al. 2008; Kittler et al. 2009). Decreased brainstem latencies for individuals with Down syndrome have been attributed to smaller auditory structures (i.e., cochlea and central auditory pathway) and shorter neural conduction times (Diaz & Zurron 1995; Ferri et al. 1995; Forti et al. 2008). Though calibration techniques have not been widely reported in the literature, assuming appropriate calibration, evidence of shortened ABR latencies for individuals with Down syndrome suggests altered responses to auditory stimuli measured at the brainstem, the first site of binaural interaction. Delays in late-latency cortical potentials to auditory stimuli suggest impairments in preattentive auditory processing for individuals with Down syndrome (Seidl et al. 1997; Pekkonen et al. 2007). Thus, electrophysiological evidence suggests that differences in neural processing of auditory stimuli exist between individuals with Down syndrome and their typically developing peers.

Behavioral Measures of Hearing in Children With Down Syndrome Prevalence estimates of hearing loss in children with Down syndrome range from 50 to 80%, which is conductive in the majority of occurrences (Shott 2006). Beyond prevalence estimates, relatively few studies have examined auditory abilities in children with Down syndrome by using behavioral techniques. However, there is some evidence suggesting auditory differences between these children and their typically developing peers (e.g., Glenn et al. 1981; Werner et al. 1996). For example, the auditory sensitivity of infants with Down syndrome has been shown to be up to 10 to 25 dB poorer than that of their typically developing peers by using behavioral techniques, despite indications of normal-hearing sensitivity from screening ABR and tympanometry (Werner et al. 1996). In addition, infants with Down syndrome prefer listening to complex auditory stimuli for longer periods of time than their typically developing peers, a difference that is not seen for simple stimuli (Glenn et al. 1981). There is very little known about what auditory perceptual deficits might exist in Down syndrome, apart from any arising from simple audiometric factors. Behavioral thresholds in auditory tasks reflect a combination of both auditory factors (e.g., binaural sensitivity) and more general, cognitive factors (e.g., attention). It is notably difficult to differentiate the contributions of these factors (e.g., Allen & Wightman 1994; Werner et al. 1996). However, examination of psychometric functions can be useful in this regard. Psychometric functions define the relationship between a stimulus parameter of interest (e.g., signal level) and percent correct. Inattention reduces the upper asymptote and the slope of the psychometric function. These hallmarks of inattention have been used previously to understand maturation of auditory processing skills in typically developing children (e.g., Allen & Wightman 1994). They could also shed light on the factors affecting the performance in children with developmental delays.

Binaural Hearing in Noise It has been well documented that the effects of interfering background noise decrease when listening with two ears rather

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than with one under many stimulus conditions (e.g., Carhart 1965; Moncur & Dirks 1967). Binaural hearing results in a number of listening advantages relative to monaural hearing, including enhanced hearing sensitivity, more accurate localization of auditory signals, and better speech understanding in adverse listening conditions. The central auditory system is able to exploit binaural difference cues to reduce the interference of background noise for a signal of interest. A typical measure of binaural release from masking is based on the detectability of pure-tone signals in the presence of noise maskers presented over headphones (e.g., Hirsh 1948). For example, detection threshold can first be measured in a reference condition in which the masker and the signal are each presented identically to the two ears (a condition referred to as N0S0). If the interaural phase relationship of the signal or masker is changed, there can be an improvement in threshold, or a release from masking. The difference in threshold between the reference condition and the dichotic configuration is commonly referred to as the masking level difference (MLD). The maximum MLD—about 15 dB for a low-frequency tone—is typically observed when the masker is presented identically to the two ears while the signal tone is presented 180 degrees out of phase in one ear relative to the other (a condition referred to as N0Sπ; see Green 1976 for a review). The ability to use interaural cues to detect signals in noise develops throughout childhood. Infants and young children have been shown to have smaller MLDs than adults for many signal and noise configurations (Nozza 1987; Hall & Grose 1990; Grose et al. 1997; Van Deun et al. 2009). For example, typically developing infants with normal hearing have smaller MLDs than adults for 500-Hz pure-tones presented in broadband noise (i.e., 600 Hz; Nozza 1987). However, by about 5 to 10 years of age, typically developing children have adult-like MLDs for similar signal and noise configurations (e.g., 500 Hz pure tones presented in broadband noise; Hall & Grose 1990; Grose et al. 1997). Similar results have been observed for filtered click trains presented in broadband noise (Van Deun et al. 2009). However, masker bandwidth can affect MLDs in children. That is, children as old as 8 to 10 years of age have smaller MLDs than adults for signals presented in narrower bandwidths of noise, such as 20 and 40 Hz (Grose et al. 1997). Binaural release from masking can also be measured for speech signals, typically by comparing the change in detection or intelligibility of speech signals in noise presented in varying binaural configurations. This can be done in the free field by spatially separating signal and noise sources or under headphones by varying parameters as in the tonal MLD paradigm or by specifically controlling interaural time difference (ITD) or interaural level difference (ILD). Several studies have demonstrated the positive effects of binaural release from masking on listening to speech in adverse listening situations for children and adults (e.g., Moncur & Dirks 1967; Bronkhorst & Plomp 1988; Nozza et al 1988; Garadat & Litovsky 2007). Advantages of 3 to 9 dB can be expected for conditions similar to real-life binaural hearing situations, in which ITDs and ILDs are available (Carhart 1965; Levitt & Rabiner 1967). Binaural advantage generally improves with age for children for speech sounds and sentences presented in noise (Nozza et al. 1988; Cameron et al. 2009). For example, infants have smaller MLDs than adults for detection of the speech sound /ba/ presented in broadband masking noise; however, adult-like

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MLDs can be obtained in this condition for children between the ages of 3.5 and 4.5 years (Nozza et al. 1988). Similarly, increased binaural advantage with age for understanding sentences presented in multi-talker noise can be obtained for children between the ages of 5 to 11 years (Cameron et al. 2009). However, children as young as 2.5 years of age have demonstrated binaural benefit similar to adults for understanding speech in noise in some circumstances (Garadat & Litovsky 2007). For example, preschool and school-age children exhibit adult-like binaural benefit for understanding closed-set spondees presented in competing speech stimuli (Litovsky 2005; Garadat & Litovsky 2007). There are two reasons that measures of binaural masking release are well suited to the study of auditory perception in children with Down syndrome. One is that the masking release depends on the ability of the auditory system to encode and process subtle ITD cues. Tests of binaural masking release have been found to be sensitive to subcortical auditory pathologies in clinical populations (e.g., Olsen et al. 1976). Structural anomalies within the central auditory system and alterations in synaptic communication could adversely affect various aspects of auditory processing for children with Down syndrome, including binaural hearing (for review, see Porter & Tharpe 2010). However, binaural hearing capabilities have not been examined in these children. A second reason that measures of binaural masking release are well suited to the study of auditory perception in children with Down syndrome is that binaural masking has been found to be reduced in children having a history of chronic otitis media with concomitant hearing loss (e.g., Hall & Grose 1993). Chronic otitis media is prevalent in children with Down syndrome, affecting approximately 70% of children with Down syndrome as compared with approximately 40% of typically developing children (Auinger et al. 2003; Mitchell et al. 2003). High rates of chronic middle ear disease for children with Down syndrome have been attributed to nasopharyngeal structure, hypotonicity, and immune deficiencies (Shott 2006). Sustained durations of auditory deprivation are likely required for negative effects to occur, as reduced binaural masking release has not been observed in 7- to 10-month-old infants with recurrent otitis media (Hutchings et al. 1992). However, once impacted, MLD can remain reduced for up to 2 to 3 years after surgical correction (i.e., tympanostomy tube placement) for some children (Hall et al. 1995). It is therefore of interest to examine binaural masking release in children with Down syndrome. The present study sought to determine whether the binaural abilities of children with Down syndrome are compromised relative to those of typically developing children. This was done using two different tasks: (1) an MLD task using 500-Hz puretone stimuli in 300-Hz wide masking noise; and (2) a binaural intelligibility level difference (BILD) task using speech stimuli in the presence of speech-shaped broadband noise. The hypothesis was that children with Down syndrome would have less binaural benefit, shown by smaller MLD and BILD than typically developing children for these experimental conditions.

PARTICIPANTS AND METHODS Participants Fifty-two typically developing children and 14 children with Down syndrome consented to participate in this study. A larger

number of typically developing children than children with Down syndrome were included in the study to facilitate comparisons between these groups based on the chronological ages, as well as estimates of the developmental ages of children with Down syndrome. All study participants had pure-tone thresholds ≤ 20 dB HL bilaterally at 500 Hz with the exception of 3 children with Down syndrome who had unilateral thresholds of 25 dB HL (n = 1) or 30 dB HL (n = 2). In addition, all participants had pure-tone threshold averages (PTAs) of ≤20 dB HL measured at 500, 1000, 2000, and 4000 Hz, with the exception of 1 child with Down syndrome and 1 typically developing child who had unilateral PTAs of 27 and 25 dB HL, respectively. Bone conduction audiometry and tympanometry were not routinely included in pre-experimental testing. Average 500 Hz thresholds and PTAs are shown in Table 1 and Table 2, respectively. Children with Down syndrome had significantly higher 500 Hz thresholds and PTAs than typically developing children (p ≤ 0.001). The potential for elevated hearing thresholds for children with Down syndrome was considered when choosing stimulus presentation levels, as discussed later in the article. Children with additional significant disabilities affecting gross motor control or a known receptive language age of less than 3 years were excluded from recruitment for this study. Six typically developing children were excluded as a result of hearing thresholds >30 dB HL (n = 1), failure to pass preexperimental feasibility testing (described later in the article; n = 3), or task refusal after consenting (n = 2). Three children with Down syndrome were excluded because of failure to pass pre-experimental feasibility testing. As such, 46 typically developing children (M = 7 years, 5 months; range = 3 years, 4 months to 12 years, 11 months), and 11 children with Down syndrome (M = 11 years, 5 months; range = 6 years, 6 months to 16 years, 11 months) were tested on all experimental conditions and included in the data analysis. Procedures described later in the article showed that a greater percentage of children with Down syndrome were reported by their parents to have a significant history of otitis media (n = 7, 64%) than typically developing children (n = 10, 22%), as anticipated. The majority of children with Down syndrome included in this study had Trisomy 21 identified by karyotype according to the medical record or parental report (81%). However, 1 child was noted to have translocation of chromosome 21 to chromosome 14, and 1 child’s karyotype information was unavailable in the medical record. The amount of developmental delay observed, using the Vineland Adaptive Behavior Scales Parent/ Caregiver Report Form (Second Edition; Sparrow et al. 2005; TABLE 1.   Hearing threshold for 500 Hz shown in dB HL, masked thresholds in N0S0 and N0Sπ conditions shown in dB SPL, and MLDs shown in dB M (SD)

TD Children (n = 46) Children with DS (n = 11) Control adults (n = 6) Adults with DS (n = 3)

500 Hz

N0S0

N0Sπ

MLD

−0.3 (4.2) 11.5 (7.6) −2.1 (2.5) 2.5 (5.0)

81.5 (6.6) 90.7 (5.9) 77.8 (5.1) 83.7 (6.9)

67.8 (9.0) 88.1 (7.6) 62.6 (5.6) 64.1 (0.9)

13.7 (4.9)   2.6 (6.7) 15.2 (3.3) 19.7 (6.2)

Associated standard deviations are shown in parentheses. DS, Down syndrome; MLD, masking level difference; TD, typically developing.



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TABLE 2.   Bilateral PTA shown in dB HL, masked thresholds for FF0, FF45, and FF90 conditions shown in dB SPL, and BILDs for the FF45 and FF90 shown in dB M (SD)

TD children (n = 46) Children with DS (n = 11) Control adults (n = 6) Adults with DS (n = 3)

PTA

FF0

FF45

FF90

BILD FF45

BILD FF90

1.1 (3.0) 11.0 (4.9) 1.3 (1.3) 7.8 (4.2)

83.1 (5.1) 88.0 (3.9) 70.4 (4.0) 80.8 (2.8)

80.2 (5.0) 85.0 (3.4) 66.8 (5.3) 79.3 (3.8)

80.4 (5.8) 85.9 (4.9) 64.9 (5.5) 81.2 (2.7)

2.9 (4.2) 3.0 (4.7) 3.6 (3.3) 1.5 (1.9)

2.7 (4.3) 2.1 (7.0) 5.5 (3.0) −0.4 (0.2)

Associated standard deviations are shown in parentheses. BILD, binaural intelligibility level difference; DS, Down syndrome; PTA, pure-tone average, defined as the mean detection thresholds at 500, 1000, 2000, and 4000 Hz in the left and right ear; TD, typically developing.

see later in this article), for children and adolescents with Down syndrome ranged from 1 year, 6 months to 9 years, 4 months (M = 4 years, 8 months, SD = 4 years, 9 months). This range does not include 1 child with Down syndrome who, via parent report, was noted to have an age-equivalent score that was 7 years, 3 months greater than chronological age. The estimate could not be verified and is considered unlikely based on the researcher’s observation of the child. In addition to the child participants, 6 control adults with no known neurological or cognitive delays (M = 27 years, 6 months; range = 23 years, 1 month to 35 years, 9 months) and 3 adults with Down syndrome (M = 28 years, 1 month; range = 22 years, 3 months to 38 years, 4 months) also consented to participate in the study so that an estimate of adult performance could be obtained for the experimental tasks. Study procedures were approved by the Institutional Review Board at Vanderbilt University Medical Center, Nashville, Tennessee. Participants with Down syndrome were recruited from the Down Syndrome Association of Middle Tennessee, the Monroe Carell Jr. Children’s Hospital at Vanderbilt Down Syndrome Clinic, the Vanderbilt Bill Wilkerson Center, and the Vanderbilt Kennedy Center.

Materials and Procedures All child and adult participants performed all tests described in this article. Auditory stimuli were presented through Sennheiser HD 265 linear headphones (Sennheiser Electronic Corporation; Old Lyme, CT) by using MATLAB 7.1 (The MathWorks, Inc.; Natick, MA) to generate and control auditory stimuli and visual reinforcement when applicable. Audio files were played using an integrated Intel sound card with a 24,414-Hz sampling rate. Visual stimuli were routed from a main computer to a secondary computer monitor used for the singular purpose of response reinforcement for paradigms in which visual reinforcement was used (i.e., audiometric testing and MLD tasks).

Pre-Experimental Procedures Parents of children and adolescents with Down syndrome were asked to complete the Vineland Adaptive Behavior Scales Parent/Caregiver Report Form (Second Edition; Sparrow et al. 2005), a measure of personal and social skills required for daily living (i.e., adaptive behavior) appropriate for individuals aged 3 years, 0 months to 21 years, 11 months. Age-equivalent scores from the receptive communication subdomain were used as an estimate of developmental ability for children with Down syndrome, as this subdomain most closely pertained to

the experimental tasks used for this study. Parents of all child and adolescent participants were asked to complete a brief survey designed to obtain demographic information regarding otologic health history. Similar to past research, a significant history of middle ear disease was defined as the occurrence of five or more episodes of middle ear disease before the age of 5 years or the surgical placement of pressure equalization tubes (Moore et al. 1991). Although not used as exclusionary criteria, otologic health history information was documented based on past research, suggesting that recurrent otitis media in early childhood can result in reduced MLD (Hall et al. 1995). Finally, before each experimental task, participants were required to demonstrate at least 80% accuracy to be included in the corresponding experimental task. Procedures for feasibility testing and experimental testing were identical with the exception that the first trial was begun at +5 dB SNR for the MLD task and +10 dB SNR for the BILD task. Feasibility testing was completed in the N0Sπ condition for the MLD task and in the FF0 condition for the BILD task.

Experimental Procedures Data Collection Parameters  •  Data were collected using a twoalternative forced-choice paradigm, and a two-down one-up adaptive procedure to estimate the 70.7% point in the psychometric function (Levitt 1971). On each trial, signal and no-signal presentations occurred in random order, and the participant indicated which presentation contained the signal. Masker level was fixed at 85 dB SPL to enable robust masking release despite the possibility of mild conductive hearing loss that often occurs in individuals with Down syndrome (Hirsh 1948). The first stimulus in each threshold estimation track was presented at 0 dB SNR. Signal level was adjusted in steps of 4 dB for the first two reversals, then in steps of 2 dB for the remaining six reversals. The mean of the last six reversals was used to estimate threshold. Two runs were administered for each MLD condition for most children and all adults included in this study. Thresholds for N0S0 and N0Sπ conditions were determined as the result of one run for each condition for 5 children with Down syndrome and 3 typically developing children due to test fatigue. When two threshold estimates were measured, the average was taken as the final threshold. One run was completed per BILD condition. Conditions were administered in random order for both the MLD task and the BILD task.

Masking Level Difference Stimuli consisted of a 500-Hz pure-tone presented either interaurally in phase (S0) or 180 degrees out of phase (Sπ). The

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masker was a 300-Hz wide Gaussian noise, centered at 500 Hz, presented interaurally in phase (N0), similar to other research (Hall & Grose 1993). The signal was 400 msec in duration with a 50-msec rise/fall time, temporally centered within a 800-msec sample of masking noise. The interstimulus interval was 400 msec and presentation of stimuli on each trial began approximately 500 msec after participant response to the stimuli on the previous trial. Participants were told a story about an owl that lived in a windy forest. The 500-Hz tone was identified as the owl’s call, and the masking noise was identified as the noise of the forest. A computer monitor was used to generate two identical forest images located on the left and right of the screen. The images were highlighted individually, left to right, and corresponded to the presentation of noise to demark temporal intervals. A series of different owl and forest images was randomly presented to increase visual interest for this task. Participants were asked to point to identify in which forest the owl was hiding. The location of the owl (i.e., correct response) was revealed after the participant’s response.

Binaural Intelligibility Level Difference Speech material consisted of recorded words from the Northwestern University-Children’s Perception of Speech test (NU-CHIPS; Elliott & Katz 1980). This test was designed for use with children whose language age is 3 years or above. Speech stimuli were between approximately 500 and 800 msec in duration, and they were presented in the context of a background noise. Noise stimuli consisted of a continuous broadband noise with the same long-term spectral average of the NU-CHIPS speech stimuli. Children heard monosyllabic words presented in noise. They were asked to identify the word they heard by pointing to one of four alternatives on black-andwhite picture plates that are included with the standard NUCHIPS test materials. Spatial location was simulated to facilitate equipment portability and allow for testing in the clinical research space adjacent to the Vanderbilt Down Syndrome Clinic. This convenience assisted with recruitment efforts and reduced family burden for participants with Down syndrome. Spatial location was simulated under headphones by using speech and noise signals that were presented from a Tannoy Precision 6P loudspeaker (Tannoy, Ltd., North Lanarkshire, Scotland) and recorded from two ER-11 microphones (Etymotic Research, Inc., Elk Grove Village, IL) placed in the ears of a Knowles Electronic Manikin for Acoustic Research (KEMAR) that was positioned in an anechoic chamber at the Vanderbilt Bill Wilkerson Center. Speech material was presented from 0-degree azimuth (i.e., directly in front of KEMAR) at a distance of 1.5 m. Noise was presented from 0-, 45-, or 90-degree azimuth by rotating the head and torso of KEMAR while keeping the position of the loudspeaker fixed. An equalization filter was applied to recordings, as described by Killion (1979). This was necessary to account for the addition of the ear-canal resonance of the listener when playing this type of recording through headphones. The noise recordings were used to create simulated free-field conditions for noise signals presented from 0 (i.e., FF0), 45 (i.e., FF45), and 90 degrees (i.e., FF90), preserving the natural ILD and ITD cues. Speech stimuli recorded at 0-degree azimuth were presented in all conditions.

RESULTS Masking Level Difference Table  1 includes means and standard deviations of detection thresholds in quiet measured at 500 Hz, thresholds for each MLD condition (i.e., N0S0 and N0Sπ), and the MLD. Thresholds for the N0S0 condition and the N0Sπ condition for individuals with Down syndrome and typically developing individuals are plotted in Figure 1. Thresholds are plotted as a function of chronological age, with age represented on a log scale to better illustrate the trend across the large age range employed in this study. The first analysis was done to compare N0S0 thresholds for children with Down syndrome, typically developing children, adults with Down syndrome, and control adults. Consideration of N0S0 threshold provides an estimate of the effects of energetic masking in the absence of the binaural ITD cue that is present for the N0Sπ condition. A univariate analysis of variance (ANOVA) including two between-groups factors (diagnostic group and age group) indicated significant main effects of diagnostic group (F[1,58]=8.96, p = 0.004) and age group (F[1,58]=4.43, p ≤ 0.04). This suggests that, in general, participants with Down syndrome had higher N0S0 thresholds than typically developing participants, and children had higher N0S0 thresholds than adults. A significant diagnostic group by age group interaction was not observed (p = 0.522), suggesting relatively similar differences in N0S0 threshold for children with Down syndrome and typically developing children as for adults with Down syndrome and control adults. In other words, the relative impact of energetic masking is similar for children and adults with Down syndrome compared with similarly aged typically developing individuals. The next analysis was done to compare the MLDs of children with Down syndrome, typically developing children, adults with Down syndrome, and control adults. Thresholds for the N0Sπ condition were subtracted from thresholds for the N0S0 condition to obtain MLDs. Table 1 provides average MLD values for all of the study groups. Figure 2 shows the MLD as a function of chronological age (plotted on a log scale), with the 95th confidence interval for control adults (95% CI [12.7, 18.6]). A univariate ANOVA indicated a main effect of age group (F[1,58]=20.36, p ≤ 0.001), suggesting that, in general, children had less binaural masking release than adults. In addition, a significant diagnostic group by age group interaction was observed (F[1,58]=14.44, p ≤ 0.001). Follow-up analyses suggested that children with Down syndrome had less binaural masking release than typically developing children (t[51]=−5.95, p ≤ 0.001, d = 1.24), but that

Fig. 1. Thresholds for N0S0 and N0Sπ conditions for typically developing (TD) individuals (open symbols) and individuals with Down syndrome (DS; filled symbols), plotted as a function of chronological age in years (with age plotted on a log scale).



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Fig. 2. Masking level difference (MLD) as a function of chronological age in years (with age plotted on a log scale) for typically developing (TD) individuals (open symbols) and individuals with Down syndrome (DS; filled symbols). The shaded area represents the 95% confidence interval for control adults.

adults with Down syndrome had binaural masking release similar to that of control adults (p = 0.184). An association between the log of age and MLD was not observed for children with Down syndrome, suggesting that MLD did not systematically vary according to age for children with Down syndrome included in this study. As such, a linear regression analysis was used to predict the age at which the average MLD of children with Down syndrome could be expected to occur for typically developing children in our data set. This analysis suggested that the average MLD of children with Down syndrome included in this study (2.6 dB) is commensurate with MLDs expected for a typically developing child aged 5.2 years. No association was observed for MLD and developmental age (i.e., Vineland Adaptive Behavior Scales receptive language age-equivalent subscale) for children and adolescents with Down syndrome, suggesting that developmental ability did not significantly influence the MLD.

Binaural Intelligibility Level Difference Table  2 includes bilateral PTA, thresholds for simulated free-field BILD conditions (i.e., FF0, FF45, and FF90), and the BILD for simulated free-field conditions (i.e., BILD FF45 and BILD FF90). Thresholds for simulated free-field conditions used for the BILD task (i.e., FF0, FF45, and FF90) are shown in Figure 3, plotted as a function of chronological age.

Fig. 3. Threshold for FF0, FF45, and FF90 conditions as a function of chronological age in years (with age plotted on a log scale) for typically developing (TD) individuals (open symbols) and individuals with Down syndrome (DS; filled symbols).

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The first analysis was done to compare FF0 thresholds for children with Down syndrome, typically developing children, adults with Down syndrome, and control adults. This provided an estimate of the effects of masking in the absence of simulated spatial release from masking cues that are present for the FF45 and FF90 conditions. A univariate ANOVA including two between-groups factors (diagnostic group and age group) indicated significant main effects of diagnostic group (F[1,61]=16.32, p ≤ 0.001) and age group (F[1,61]=27.83, p ≤ 0.001). This suggests that, in general, individuals with Down syndrome had higher masked thresholds for speech than typically developing individuals and that children had higher masked thresholds for speech than adults. A significant diagnostic group by age group interaction was not observed (p = 0.15), suggesting similar relative amounts of masking for children and adults with Down syndrome compared with similarly aged typically developing individuals. Thresholds for simulated free-field conditions at FF45 and FF90 were subtracted from FF0 to calculate BILD FF45 and BILD FF90, respectively. These conditions provided an estimate of masking release experienced by simulated separation of a speech signal from a noise masker by 45 degrees (BILD FF45) and 90 degrees (BILD FF90). Separate univariate ANOVAs with BILD FF45 or BILD FF90 as dependent variables indicated no main effect of diagnostic group or age group and no significant diagnostic group by age group interaction (p ≥ 0.05). This suggests that the masking release experienced for simulated spatial separations of 45 degrees and 90 degrees was similar for children with Down syndrome, typically developing children, adults with Down syndrome, and control adults for the experimental parameters used in this study. Developmental age was not associated with spatial release from masking for either condition for any group, suggesting cognition did not significantly influence BILD for individuals with Down syndrome.

Psychometric Functions As previously mentioned, behavioral thresholds are influenced by both auditory (e.g., binaural ability) and cognitive (e.g., attention) factors. Detrimental cognitive influences on behavioral thresholds, such as inattention, are reflected in lower asymptotes and shallower slopes of the psychometric function. Though this study was not specifically designed to obtain data to compile detailed psychometric functions, the psychometric function slope obtained during threshold estimation was estimated to provide insight into the relative influence of attention on task performance (Leek et al. 1992). This was achieved by analyzing the signal level and listener response on each trial of an adaptive track. Signal levels for trial-by-trial data for the MLD and BILD tasks were normalized by participant threshold (i.e., normalized signal level = signal presentation level – participant threshold). Results were summed by group, inventoried according to number of points per coordinate, and psychometric functions were fit to data according to methods and software described in the study by Wichmann and Hill (2001). Slope was defined in terms of the k-parameter in the following equaa , where a is the maximum y value, tion: f ( x ) = 1 + −( x − µ )/ k 1+ e μ is the midpoint of the function, and k is the slope parameter. Upper asymptote was fixed at 100% due to the relatively small number of data points obtained at asymptote. Psychometric functions for N0S0, N0Sπ, FF0, and FF90 conditions for

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children with Down syndrome and typically developing children are shown in Figure 4. Children with Down syndrome and typically developing children had similar psychometric function slopes for the N0Sπ (Down syndrome, k=4.18; typically developing, k = 4.96), FF0 (Down syndrome, k=3.24; typically developing, k = 3.65), and FF90 (Down syndrome, k = 3.57; typically developing, k = 3.14) conditions. For the N0S0 condition, children with Down syndrome had a somewhat shallower psychometric function slope (k = 5.13) than typically developing children (k = 3.32). Thus the slopes of group psychometric functions suggest that attentiveness and motivation contributed equally to performance for most tasks for children with Down syndrome and typically developing children.

DISCUSSION Results from the present study align well with past studies that have examined MLD for adults and children and BILD for adults (e.g., Hirsh 1948; Bronkhorst & Plomp 1988; Hall & Grose 1990; Moore et al. 2011). First, average MLD for control adults in the present study was 15.2 dB, which is consistent with past results of MLDs of 15 dB for adult listeners with normal hearing for low-frequency pure-tone signals (Hirsh 1948). In addition, the average MLD for typically developing children in this study was 13.7, which is similar to past findings regarding MLDs of approximately 13 to 16 dB for typically developing children obtained using similar paradigms to the present study. Also similar to past research, MLD improved with age for typically developing children (Hall & Grose 1990; Moore et al. 2011). With respect to the BILD task, average SNR at threshold for the simulated free-field condition at 90 degrees (i.e., FF90) was −17.3 dB for control adults in the present study, similar to the average SNR at threshold of −16.6 dB obtained by Bronkhorst and Plomp (1988) for this condition. Though Bronkhorst and Plomp did not include a simulated free-field condition at 45 degrees, the average across the reported SNR threshold for 30 degrees and 60 degrees was −14.3 dB, similar

to the present average SNR threshold result of −15.3 dB for the 45-degree condition. Similarities between results from the present study and past results validate this research paradigm, particularly the methods used for simulating free-field test conditions. However, some differences were noted between results from the present study and that of Bronkhorst and Plomp. For example, average SNR at threshold for the simulated free-field condition at 0 degree was −11.8 dB for the control adults in the present study, which represents better speech recognition in noise than the −6.4 dB reported for this condition by Bronkhorst and Plomp. Speech recognition scores in our study could have been better than those in the study by Bronkhorst and Plomp in this instance due to methodological differences. We employed a closed-set monosyllable word identification task, which is easier than the open-set sentence recognition task used by Bronkhorst and Plomp. Results of the present study suggest poorer binaural auditory abilities for children with Down syndrome compared with similarly aged, typically developing children. Despite normal to near-normal pure-tone sensitivity, children with Down syndrome in this study had smaller MLDs than typically developing children. This result is consistent with the idea that cues resulting in release from masking for typically developing children, such as ITD cues, benefit children with Down syndrome to a lesser extent. These effects are thought to be related to binaural ability and not attributable to developmental delay for a few reasons. First, any nonbinaural influences, such as those related to cognition, can be assumed to impact threshold for both the N0S0 and N0S conditions equally, effectively negating the influence in calculations of the MLD. Next, developmental age was not associated with MLD for children with Down syndrome, suggesting that general attention or cognition did not significantly influence MLD for these children. Finally, similarities in the slopes of group psychometric functions for children with Down syndrome and typically developing children suggest that attentiveness and motivation contributed equally to the performance of both groups of children for most tasks.

N0Sπ

N0S0

FF0

FF90

Percent Correct

Children with DS

100

50

0

TD Children

100

50

0 −20

0

20

−20

0

20

−20

0

20

−20

0

20

Normalized Level (SPL/∆SPL)

Fig. 4. Percent correct as a function of normalized threshold for N0S0, N0Sπ, FF0, and FF90 for children with Down syndrome (DS) and typically developing (TD) children. Symbol size represents relative number of data points per coordinate. Curves represent best fitting logistic functions.



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Though MLDs were smaller for children with Down syndrome relative to typically developing children, no difference in MLD was observed for adults with Down syndrome and control adults. This suggests immaturities in this process for children with Down syndrome relative to typically developing children, which do not necessarily persist into adulthood. Children with Down syndrome in this study were approximately 11 years of age on average, but were estimated to have MLDs equivalent to typically developing children aged 5.2 years. This represents a substantial delay for children with Down syndrome relative to their typically developing peers. Considering the high prevalence of otitis media and associated conductive hearing loss in children with Down syndrome, it is possible that the development of binaural hearing for children with Down syndrome included in this study could have been impacted by past conductive hearing loss secondary to otitis media. In typically developing children, otitis media with effusion has been shown to influence the development of the MLD (Hall & Grose 1993) and that the effects can last for as long as 2 years after surgical correction to remedy the impairment (Hall et al. 1995). Although chronic otitis media could have contributed to the results observed for children with Down syndrome in the present study, sufficient numbers of children were not included to evaluate this effect. Another explanation could be that there is a subtle difference between adults with Down syndrome and control adults, and the small number of adults included in this study precluded seeing a significant effect. However, all adults with Down syndrome in the present study had MLDs equal to or larger than those reported in the literature for normal-hearing nonsyndromic adults (Hirsh 1948), suggesting a trend that might continue with more data collection. Additional insight regarding potential sources of differences observed between individuals with Down syndrome and typically developing individuals might be found in past studies that have examined electrophysiologic test results. For example, results from ABR testing have been associated with the magnitude of behavioral MLDs for typically developing children and adults with neurologic impairments (Noffsinger et al. 1982; Hannley et al. 1983). Smaller MLDs have been associated with poor integrity of ABR waves I, II, and III (Noffsinger et al. 1982; Hannley et al. 1983). Considering differences noted in previous research between ABR test results for individuals with Down syndrome and typically developing individuals (Folsom et al. 1983; Forti et al. 2008), it is possible that the smaller MLDs observed for children with Down syndrome in this study might have been influenced by brainstem processing of auditory signals. Furthermore, large interaural asymmetries of interpeak latencies I to III and I to V have been associated with smaller MLDs for children with a history of otitis media (Hall & Grose 1993), a condition prevalent in children with Down syndrome, as previously discussed. Differences in simulated spatial release from masking were not observed for individuals with Down syndrome and typically developing individuals on this task. These findings were unexpected and might have been influenced by the task parameters used for this study. Recall that we used a closed-set monosyllabic task developed for use with children as young as 3 years of age. Relatively good speech recognition in the most difficult listening condition could have resulted in less relative improvement in speech recognition as listening conditions improved. Indeed, results from control adults included in the present study were better than those found by Bronkhorst and Plomp for the most difficult listening condition (i.e., FF0), but were relatively

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similar for conditions in which the signal and noise were spatially separated. In addition, BILD scores represented a wide range of performance. These scores could have been influenced by the use of a single run per condition. Use of multiple runs per condition, including within-condition between-run variability criteria, could have resulted in more precise estimates of threshold than presently observed and possibly reduced the range of BILD results. Finally, the use of nonindividualized head-related transfer functions (HRTFs) could have resulted in subjects hearing the signals internalized, rather than externalized. Past research has shown adequate performance using estimated HTRFs and simulated free-field conditions, at least for adults and children with no known neurological impairments (Bronkhorst & Plomp 1988; Cameron et al. 2009). However, individuals with Down syndrome have unique structural characteristics of the outer ear and ear canal, and the potential effect of nonindividualized HRTFs should not be dismissed. This study examined binaural masking release for children with Down syndrome by using methods that have been shown to be sensitive to developmental effects in release from masking. It would be of interest to examine other auditory abilities in children with Down syndrome. For example, frequency and temporal resolution contribute to detecting signals in noise and are important for speech understanding (for review, see Phillips 1999; Buss et al. 2012). It is possible that insufficiencies in these processes contributed to the elevated masked thresholds and reduced binaural benefits observed for children with Down syndrome relative to typically developing children in this study. However, central factors, such as sustained attention and listening efficiency, also contribute to children’s performance (Hall & Grose 1991; Moore et al. 2008). Studies to explore these capabilities should be undertaken to determine their influence on hearing thresholds in noise for individuals with Down syndrome.

CONCLUSIONS Despite normal to near-normal hearing sensitivity, children with Down syndrome had poorer thresholds in noise than typically developing children. Furthermore, children with Down syndrome experienced less masking release for pure-tone stimuli than typically developing children, but adults with Down syndrome and control adults had similar MLDs. This suggests a delay in release from masking abilities for pure-tone stimuli for children with Down syndrome rather than an absolute deficit in this area. The reduced binaural benefit experienced by children with Down syndrome suggests that they will require more favorable SNRs than typically developing children to achieve optimal performance in adverse listening conditions. This could have important implications for the planning of educational and therapeutic interventions for individuals with Down syndrome.

ACKNOWLEDGMENTS The authors thank Emily Buss for her able assistance with psychometric function calculations and for her comments on an earlier version of this article. The authors are also grateful to John Grose and Joseph Hall for their insightful comments on a previous version of this article. This work was supported in part by a grant from the Special Olympics, Inc. and the U.S. Department of Health and Human Services, Centers for Disease Control and Prevention. The authors declare no other conflict of interest.

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Address for correspondence: Heather L. Porter, Department of Otolaryngology—Head and Neck Surgery, University of North Carolina at Chapel Hill, 170 Manning Drive, Chapel Hill, NC 27599, USA. E-mail: [email protected]. Received March 21, 2013; accepted November 26, 2013.

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