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. Author manuscript; available in PMC: 2023 Mar 1.
Published in final edited form as: Ear Hear. 2021 Jul 7;43(2):347–360. doi: 10.1097/AUD.0000000000001098

Variation in auditory experience affects language and executive function skills in children who are hard of hearing.

Ryan W McCreery 1, Elizabeth A Walker 2
PMCID: PMC8738778  NIHMSID: NIHMS1714357  PMID: 34288630

Abstract

Objective:

Children who are hard of hearing (CHH) experience delays in spoken language and executive function, but the mechanisms for these deficits remain unresolved. Differences in auditory experience and language skills have been examined as contributing factors to deficits in executive function, primarily with children who are deaf and children with cochlear implants. The theoretical model of cumulative auditory experience quantifies auditory dosage as how much speech is audible and how often children wear their hearing aids. CHH with higher auditory dosage have better language outcomes than peers with less auditory dosage. However, the effects of auditory experience on executive function has not been studied in CHH. The goal of this study was to examine the influences of auditory experience and language skills on the development of executive function in CHH.

Design:

We collected measures of aided speech audibility, hearing aid use, executive function, and receptive vocabulary in 177 CHH and 86 children with typical hearing who were 5–10 years-old and matched for socioeconomic status and nonverbal intelligence. Auditory dosage was calculated by combining each child’s average hours of hearing aid use with their audibility for speech to create a variable that quantifies individual differences in auditory access.

Results:

CHH had lower receptive vocabulary and deficits in executive function related to working memory and selective attention compared to peers with typical hearing. CHH with greater auditory dosage had higher receptive vocabulary than CHH with lower auditory dosage. Better receptive vocabulary was associated with better scores on executive function measures related to working memory and attention. Auditory dosage was also directly associated with measures of verbal working memory.

Conclusions:

CHH have deficits in language and some, but not all, areas of executive function related to working memory and attention. Auditory dosage was associated with language abilities and verbal working memory. Language was associated with individual differences in executive function skills related to attention and working memory. These results provide support for systems theories regarding the development of executive function in CHH. Interventions that improve auditory access and language may be effective for improving executive function related to working memory and attention in CHH.

Keywords: Executive function, working memory, language, hearing loss, hearing aids, audibility

Introduction

Childhood hearing loss negatively impacts language acquisition (Ching et al. 2010; Tomblin et al. 2014; Tomblin et al. 2015; Ching et al. 2017) and executive function abilities (Conway et al. 2009; Willis et al. 2014; AuBuchon et al. 2015; Nittrouer et al. 2017). Executive function refers broadly to the active control of cognitive and behavioral processes that supports planning and goal-driven behavior (Barkley, 2012; Kronenberger & Pisoni, 2020). Executive function is often thought to include at least three core components of working memory, attention switching, and inhibitory control (Miyake et al. 2000). Early deficits in executive function for children who are deaf or hard of hearing can cascade into later challenges in reading (Fagan et al. 2007; Halliday & Bishop, 2005; Park et al. 2013; Pimperton et al. 2016; Tomblin et al. 2019) and other academic skills (Tomblin et al. 2020). Given the need to account for individual differences in executive function, researchers have proposed a variety of theoretical models to examine the relative influences of and interactions between auditory (Conway et al. 2009) and language (Botting et al. 2017; Marshall et al. 2015; Hall et al. 2018a) experience on executive function skills in children with hearing loss. Many studies have examined these theories in children who are deaf and use cochlear implants and/or sign language, but less is known about how auditory experience and language skills influence executive function in children who are hard of hearing (CHH) who have bilateral mild to severe degrees of hearing loss. CHH have more residual hearing and increased variability in auditory experience compared to children who are deaf. They also show variability in language skills (Tomblin et al., 2015). The goal of this study was to examine the relative influences of auditory experience and language skills on executive function in CHH.

Executive function in children with typical hearing and CHH

Executive function refers to cognitive abilities that include temporary storage and sequencing of sensory input (working memory), inhibition of irrelevant information, and cognitive flexibility (Miyake et al. 2000; Zelazo & Müller, 2002). Executive function begins to emerge in the early preschool years (Wiebe, Espy, & Charak, 2008) and continues to develop through adolescence (Lee, Bull, & Ho, 2013). In typically developing children, executive function skills form a crucial foundation for academic achievement (Blair & Diamond, 2008; Best, Miller & Naglieri, 2011), reading (Altemeier, Abbott, & Berninger, 2008; Nouwens, Groen, & Verhoeven, 2016; Ober et al. 2019), adaptive behavior (Hofmann, Schmeichel, & Baddeley, 2012), and language acquisition (Vygotsky & Luria, 1994; Gioia et al. 2002; Fuhs & Day, 2011). Executive function and language abilities are often described as having a reciprocal relationship during development (Bishop, Nation, & Patterson, 2014, but also see Gooch et al. 2016). The importance of executive function for such a wide range of developmental areas has fueled an interest in identifying contributing factors that influence executive function skills during early childhood in the fields of developmental and cognitive psychology.

Compared to peers with typical hearing, children who are deaf and CHH often have deficits in components of executive function, including working memory (Pisoni & Cleary, 2003; Briscoe, Bishop, & Norbury, 2001; Willis et al. 2014; AuBuchon et al. 2015; Nittrouer et al. 2017; Davidson et al. 2020) and sustained attention (Dye, Hauser, & Bavelier, 2009; Dye & Hauser, 2014; Figueras et al. 2008; Hintermair, 2013; Khan, Edwards, & Langdon, 2005). There are multiple prevailing theoretical accounts that have been proposed to explain differences in executive function between children with typical hearing and children who are deaf. The primary theoretical frameworks in this area fall into three general categories with respect to the primacy and directionality of the relationships between auditory experience, language, and executive function. Auditory-based theories, including the auditory scaffolding hypothesis, suggests that early auditory deprivation leads to executive function deficits, based on evidence that children who are deaf exhibit deficits in executive function related to working memory and attention (Conway et al. 2009; Kronenberger et al. 2013). Language-based theories, on the other hand, predict that limited access to language input leads to executive function deficits (Hall, 2018b). Support for language-based theories is based on evidence that deaf children who have access to sign language and experience typical trajectories of visual language development have comparable executive function to children with typical hearing (Hall et al. 2018a). Some longitudinal studies offer further evidence to support language-based theories, in that early language abilities predict later executive function in CHH, but early executive function does not predict later language (Jones et al. 2020). However, other studies have documented deficits in executive function for children who are deaf or use cochlear implants that are not associated with language abilities (Remine, Care, & Brown, 2008). More recently, systems-based theories, including the Biopsychosocial systems theory (Kronenberger & Pisoni, 2020) and Intersubjectivity Scaffolding Hypothesis (Morgan & Dye, 2020), have been developed to acknowledge the potential for reciprocal interactions between individual and environmental factors that are likely to influence development of language and executive function. Unlike earlier auditory- or language-based accounts that suggest that either auditory or language experience primarily influences executive function development, systems-based theories acknowledge that relationships between these three domains are complex and inter-related. Biopsychosocial Systems Theory (see Kronenberger & Pisoni, 2020 for review) focuses on broad influences of genetic, environmental, and neurobiological factors, whereas the Intersubjectivity Scaffolding Hypotheses (see Morgan & Dye, 2020 for review) is oriented towards examining the impact of reciprocal interactions between children and their caregivers on the development of executive function. Nearly all the previous research that forms the basis for these theoretical perspectives has been based on children who are deaf or use cochlear implants.

Although CHH represent almost 70% of the population of children with hearing loss in the U.S. (CDC, 2020), relatively few studies have examined the effects of auditory experience, language skills or their interactions on executive function in CHH who use hearing aids. Severe or profound degrees of hearing loss that are common among children who are deaf or use cochlear implants completely limits natural auditory input. The lack of auditory input creates a stark contrast to test hypotheses about the effects of auditory experience on executive function, which may help to explain why children who are deaf or use cochlear implants have been the primary population of interest in studies of executive function development. In contrast to children who are deaf or those who use cochlear implants, CHH have better and more variable residual auditory access depending on their degree of hearing loss and the level of audibility provided by hearing aids (McCreery et al. 2015). If auditory experience is a driver of executive function skills as predicted by auditory-based theories, CHH with more auditory experience should also have better executive function than children with poorer auditory experience and relative to previous studies of children who are deaf or have cochlear implants (e.g. Pisoni & Cleary, 2003; Figueras et al. 2008). However, the effects of variation in auditory experience on executive function among CHH has not been evaluated empirically to date, despite the fact that the individual differences in auditory experience and language in this population provide an interesting opportunity to test the weighting of these factors on the development of executive function.

The few studies of executive function in CHH have produced mixed results. Two studies have shown verbal working memory deficits in CHH compared to peers with typical hearing, suggesting that even children with a mild degrees of hearing loss experience differences in executive function compared to peers with typical hearing (Briscoe et al. 2001; Willis et al. 2014). Figueras and colleagues (2008) reported poorer performance for CHH who wore hearing aids (n = 25) than age-matched peers with typical hearing on attention and cognitive flexibility measures. Conversely, Stiles and colleagues (2012) indicated that CHH (n =18) who used hearing aids had verbal and visuospatial working memory and sustained attention abilities that were comparable to their peers with typical hearing. The mixed findings in these studies could reflect the influence of individual differences in auditory experience on executive function, but that relationship was not directly addressed. Due to small sample sizes in the previous work, multivariate statistical approaches could not be used to assess the relative influences of auditory experience and language on executive function. CHH have shown varying results with regard to the relationship between language and executive function. Figueras and colleagues (2008) found an association between executive function and language, but individual differences in auditory access were not quantified beyond the group level. In a study that included CHH who used hearing aids and children who used cochlear implants, Remine and colleagues (2008) did not find an association between language and non-verbal measures of executive function. The mixed results of these studies leave primary questions about direct and indirect associations between auditory experience, language, and executive function unanswered.

The effects of language and auditory experience on executive function

Children with typical hearing show a strong association between language and executive function generally (e.g., Fuhs & Day, 2011) and working memory specifically (e.g., Gathercole & Baddeley, 2014). Evidence to support the importance of language on executive function in children with hearing loss is based on studies with children who are deaf (Botting et al. 2017; Marshall et al. 2015; Hall et al. 2018a; Hall, 2020). Recently, Jones et al. (2020) examined a mixed group of children who were deaf and CHH and showed that early language abilities predict later executive functions, but early executive function was not associated with later language abilities, lending support to the primacy of language as a driving factor for executive function (Jones et al. 2020). Despite little to no access to sound, children who are deaf and use sign language as their first language perform comparably to hearing peers in sustained and selective attention (Dye & Hauser, 2014), and parent ratings of working memory and executive function (Hall et al. 2016). Nittrouer and colleagues (2017) also found an association between vocabulary and working memory skills in deaf children who use cochlear implants. In that study, the age at which a child received their cochlear implant did not correlate with differences in verbal working memory, suggesting that differences in the length of auditory experience were not associated with working memory development. Collectively, these results lend general support to language-based theoretical accounts of the development of executive function in children who are deaf or use cochlear implants (Hall, 2018b). However, these studies do not account for the impact of individual differences in auditory experience on language and executive function.

Studies that have examined the effects of language on executive function in CHH with varying degrees of hearing loss did not directly quantify the influence of auditory experience on language or on executive function (Jones et al. 2020). The presence of substantial variation in language (Tomblin et al. 2015) and auditory experience (McCreery et al. 2015; Walker et al. 2015) for CHH could allow for a direct comparison of the relative influence of these factors on executive function skills. Children with cochlear implants have more consistent device use (Moeller et al. 2009; Park et al. 2019) than children who use hearing aids (Walker et al. 2015). There is also evidence that children who receive cochlear implants have better language skills at age 3 than CHH who use hearing aids (Ching et al. 2013), which could lead to different patterns in CHH than have been observed in previous studies of children who receive CI. Individual differences in auditory experience and language skills among CHH may be one reason that group-level comparisons of executive function for CHH in previous studies have reported inconsistent findings (e.g., Stiles et al. 2012) when compared to the consistent group differences for children who are deaf or use cochlear implants (e.g., Figueras et al. 2008; Pisoni & Cleary, 2003). Many studies of executive function and language in children who are deaf or CHH have also been confounded by small samples or group differences in age, nonverbal intelligence, or other confounding factors. Examination of auditory experience and language abilities on executive function among CHH also could provide support for systems-based theoretical accounts. Factors that influence auditory and linguistic experience for CHH, including the amount of time a child wears their hearing aid (Walker et al. 2015), how well the hearing aids are fitted (McCreery et al. 2015), and the home or family environment (Holt et al. 2020), represent potential interactions between the child’s development and their experiences and environment that have not been directly explored in previous studies.

A recent line of research has sought to develop a framework for quantifying the cumulative auditory experience of CHH (Moeller & Tomblin, 2015). The cumulative auditory experience model is based on findings that the auditory input that a child with hearing loss receives depends on their degree of hearing loss (McCreery et al. 2013), level of speech audibility that is restored by their hearing aids (McCreery et al. 2015), and the amount of time that hearing aids are worn (Walker et al. 2015). Each of these factors varies across CHH. Measures of auditory experience have been informative in our previous research for examining cross-sectional effects (McCreery et al. 2017; Walker et al. 2019) and longitudinal growth in language (Tomblin et al. 2015) and academic outcomes (Tomblin et al. 2020). Speech audibility and hearing aid use were associated with language growth between 2 and 6 years of age for CHH, even after controlling for degree of hearing loss (Tomblin et al. 2015). In subsequent studies, our team has developed metrics of auditory experience that weight the child’s audibility with their hearing aid (if present) with the amount of time that the child wears their device (e.g. Tomblin et al. 2020; Walker et al. 2020). For the purposes of this study, we developed a novel measure of auditory experience that weights each child’s hours of hearing aid use by the amount of speech audibility that they can access with and without amplification.To our knowledge, the effect of individual differences in auditory dosage on executive function in children has not been examined. In addition, the analyses benefitted from comparisons between CHH and a group of children with typical hearing who were matched for age, socioeconomic status, and nonverbal intelligence that have been challenging to accomplish in previous studies.

Current study

This study sought to examine whether auditory experience and language skills were associated with executive function in CHH. We evaluated the following research questions:

  1. Do CHH differ from peers with typical hearing in terms of language and executive function skills? Based on previous research, we predicted that CHH would have poorer language and executive function than peers with typical hearing matched for age and socioeconomic status.

  2. To what extent are individual differences in executive function associated with auditory dosage and language skills in CHH? We predicted that auditory dosage would be positively associated with language for CHH, and that language ability would be positively associated with executive function based on our previous research and studies that have examined these factors previously.

The results of this study will inform systems-based theoretical accounts of the effects of hearing loss on executive function. These results will also inform clinical auditory and language interventions to support executive function skills for CHH.

METHODS

Participants

Two-hundred sixty-three children who were part of the longitudinal Outcomes of Children with Hearing Loss (Moeller & Tomblin, 2015) studies contributed data for these analyses, including 212 CHH and 86 children with typical hearing. Inclusion criteria for CHH included bilateral, mild to severe hearing loss, spoken English as the primary language spoken in the home, and no additional developmental disabilities. Children who received cochlear implants during the study were not included in this analysis. Children with typical hearing were recruited to match the sample of CHH in age, socioeconomic status, and nonverbal intelligence. Children with typical hearing had hearing thresholds at 20 dB HL or better from 500 Hz – 4000 Hz at the time of the study. Table 1 summarizes the characteristics of the children who contributed data in this manuscript. Children were recruited from 16 U.S. states by three research centers involved in the longitudinal studies: Boys Town National Research Hospital (Omaha, NE), University of Iowa (Iowa City, IA) and University of North Carolina (Chapel Hill, NC). The study visits reported in these analyses occurred near the child’s 5th or 6th birthday or during the summer following 1st, 2nd, 3rd, or 4th grade. For children with measures from multiple visits during the longitudinal study, this analysis includes data from the earliest visit for each child. The average age at the time of the study visit used in these analyses was 9.3 years (range 6.5 – 11.5 years). Children and families received monetary compensation and prizes for their participation in the study. Procedures were approved by the Institutional Review Boards at each of the three research centers.

Table 1 –

Participant characteristics

Group CTH CHL
Number 86 212
Sex Female = 46, Male =40 Female = 99, Male = 113 Χ2=0.87, p = .34
Maternal education level 15.8 years of education 15.5 years of education p = 0.38
Race White = 81%
Black or African American = 4%
More than one race = 11%
Asian = 1%
Other = 2%
Not reported =1%		 White = 80%
Black or African American = 8%
More than one race = 6%
Asian = 2%
Other = 3%
Not reported =1%
Ethnicity Hispanic or Latino = 20%
Not Hispanic or Latino = 80%		 Hispanic or Latino = 16%
Not Hispanic or Latino = 84%
Age of identification N/A Mean= 17.1 months,
SD = 21.6 months,
Median = 4 months
Hearing aid (HA) N/A n= 199, 93.8%
Age of HA fitting N/A Mean = 20.6 months
SD = 22 months
Median = 7 months
Better-ear PTA N/A Mean = 45.6 dB HL
SD= 15.3 dB
Median = 45 dB HL
Aided speech audibility (SII) N/A Mean = 0.77
SD= 0.15
Median = 0.83
Average hours of HA use per day N/A Mean = 9.7 hours
SD = 3.9 hours
Median = 10.1 hours
Dosage N/A Mean = 9.9
SD = 4.4
Median = 9.3
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CTH = Children with Typical Hearing; CHL = Children with hearing loss; HL = Hearing Level, PTA = Pure-tone average hearing thresholds at 500 Hz, 1000 Hz, 2000 Hz , and 4000 Hz; SII = Speech-intelligibility index for average speech (60 or 65 dB SPL) at one meter with hearing aids; Hearing aid use based on hearing aid data logging or parent report.

Materials

Executive function measures

The executive function measures included questionnaires and behavioral measures focused on inhibition, attention, and working memory and were completed at the 1st, 2nd, 3rd, or 4th grade visits. Behavioral Rating Inventory of Executive Function (BRIEF; Gioia et al. 2000) is a parent-report questionnaire. Higher scores on the BRIEF are associated with greater difficulty in a specific domain. The Inhibit and Shift subscales were used as indices of the parents’ ratings of their child’s impulse control and cognitive flexibility or attention switching, respectively. The Auditory Attention and Response Set subtests of the NEPSY-II (Brooks et al. 2009) are norm-referenced, standardized scales of sustained attention and inhibition, respectively. Working memory measures included the working memory subscale of the BRIEF parent-report questionnaire, which assesses parent’s ratings of the child’s working memory and attention in everyday situations, and behavioral subtests from the Automated Working Memory Assessment (AWMA; Alloway, 2008). We included AWMA subtests that required short-term memory storage and storage plus processing to represent working memory tasks of varying complexity. We included verbal and visuospatial subtests to determine whether deficits varied across sensory presentation modality (e.g., Davidson et al. 2020). These subtests include Block Recall (visuospatial short-term storage), Nonword Recall subtest (verbal short-term storage), Listening Recall (verbal short-term storage plus processing), and Odd-One-Out (visuospatial short-term storage plus processing). Higher scores on the NEPSY-II and AWMA are associated with better performance on the test for a specific construct.

Language measures

The Peabody Picture Vocabulary Test-4 (PPVT; Dunn & Dunn, 2007) was used to measure receptive vocabulary at either the 1st or 3rd grade visit. The PPVT is a picture identification task where the child hears a word and must point to the picture of the word from a set of four pictures. The PPVT was selected to represent overall language abilities as this measure has been shown in previous studies to correlate strongly with other measures of spoken language with this sample (Tomblin et al. 2015) and in other independent samples (Tomblin et al. 2014).

Auditory access and auditory dosage measures

Each child participated in standard pure tone audiometric assessment at each study visit. For children fitted with hearing aids, acoustic measurements of the hearing aid in the child’s ear canal were completed using a probe microphone or simulated in a hearing-aid verification coupler using a measured or average estimate of the child’s ear canal acoustics. The Speech Intelligibility Index (SII; ANSI S3.5-1997) was applied to hearing aid verification data to estimate the audibility of speech with the hearing aid based on the child’s hearing thresholds. The SII represents the child’s access to an average speech signal (60 or 65 dB SPL) from a distance of one meter. The number of hours of hearing aid use was measured using parent report of amount of daily hearing aid use. Parent report was selected instead of data logging in the hearing aid as these measures show strong correspondence in our previous research (e.g. Walker et al. 2013) and a larger number of children had parent report data than had data logging. To measure the cumulative effect of unaided hearing and treatment intensities (i.e., aided audibility and HA use) in CHH, we calculated auditory dosage, conceptually based on previous research quantifying the dosage or intensity of language intervention at the individual level (Warren et al. 2007). To create a weighted estimate of auditory dosage, the number of hours of hearing aid use is exponentiated by each child’s aided audibility and the remaining unaided hours (24 hours – average hours of use) are exponentiated by each child’s unaided audibility. The use of a 24-hour period rather than an estimate of waking hours was used to provide a consistent reference for hours of hearing aid use per day across children as individual estimates of average sleep time for each child were not collected as part of this study, and a small number children had high estimates of hearing aid use (> 20 hours) that suggested they may wear their hearing aids while they were asleep. Auditory dosage equals Daily HA Use hours Aided Better-ear SII + (24 – Daily HA Use hours) Unaided Better-ear SII. For a child with typical hearing who does not wear hearing aids, the dosage level equals 24 (0 use hours + 241). For children who wear hearing aids, the dosage levels represent the amount of time aided and unaided weighted by the child’s audibility with and without hearing aids.

Nonverbal intelligence

The Weschler Abbreviated Scale of Intelligence 2nd Edition (WASI-II; Weschler, 2011) Matrix Reasoning and Block Design subtests were used as indices of nonverbal intelligence. The Matrix Reasoning subtest requires the child to view an incomplete visual matrix design and select an option that correctly completes the visual matrix. The Block Design subtest measures abstract visual reasoning and requires the child to use blocks with varying combinations of shapes to match a visual example within a specified time limit. These subtests were completed at enrollment in the study or 6 years of age.

Procedures

All study visits were completed in a sound-treated audiometric test room or sound-treated mobile van. Measures were administered and scored by an experienced pediatric audiologist or speech language pathologist. CHH completed all measures except audiometry while wearing their personal hearing aids at normal use settings, if applicable. Study visits lasted approximately 4 hours including breaks to minimize fatigue. Audiology and hearing aid measures were completed first, followed by measures of language and executive function.

Statistical analysis

All statistical analyses were completed in the R language for statistical computing (R Core Team, 2020). We calculated descriptive statistics for each of the demographic and outcome variables. For all analyses, data were from the child’s earliest study visit with measures of language, executive function, and auditory dosage. Children with missing data for specific variables were excluded from analyses including those variables. We used linear regression models to assess differences between children with typical hearing and CHH on each outcome measure and to analyze differences in outcomes between male and female children. For measures of executive function, Pearson correlations were first conducted to assess the associations between auditory dosage on language and on executive function, and the relationship between the effect of language on executive function. We then used linear regression models to evaluate the relationships between auditory dosage, language, and executive function skills. These factors were evaluated simultaneously because of the established associations between these variables in the previous literature and the research questions of the study. Normative standard scores or scaled scores for language and executive function were used in all statistical analyses. All models were inspected for normality by examining the distribution of model residuals. All reported p values were adjusted using the False Discovery Rate (Benjamini & Hochberg, 1995) to minimize the potential for Type I error across multiple statistical tests.

Results

Table 2 summarizes the performance on standardized measures of nonverbal intelligence, language, and executive function for children with typical hearing and CHH. There were no significant differences between male and female children on any of the outcome measures. Children with typical hearing had higher standard scores for PPVT (receptive vocabulary) than CHH. For working memory measures, children with typical hearing had higher standard scores on working memory subscales including the AWMA Nonword Recall (verbal short-term storage), Listening Recall (verbal storage and processing), and Odd-One-Out (visuospatial storage and processing) than CHH. Children with typical hearing also had lower (better) parent ratings of working memory on the BRIEF working memory subscale (working memory and attention in everyday situations) and higher scaled scores on the NEPSY Response Set measure (inhibition of attention). There were no significant differences between children with typical hearing and CHH on the WASI Matrix Reasoning or Block Design (nonverbal intelligence), BRIEF Inhibit subscale (behavioral impulse control), BRIEF Shift subscale (cognitive flexibility/attention switching), AWMA Block Recall (visuospatial storage) or NEPSY Auditory Attention (sustained attention) subscales.

Table 2 –

Comparisons of children with typical hearing and children with hearing loss on working memory and executive function measures

CTH (n = 86) CHL (n =212) Model Statistics Group difference Sex difference
WASI Matrix Reasoning t-score Mean = 56.4
SD= 9.6		 Mean = 54.6 SD=10.4 F(2,206)=0.71, p =0.48 d = −0.17 d = 0.06
WASI Block Design t-score Mean = 52.3
SD = 8.7		 Mean = 52
SD = 9.4		 F(2,206)=0.03, p=0.39 d = −0.04 d = 0.18
PPVT Standard Score Mean=114.5
SD =12.7		 Mean= 105.1
SD = 16.4		 F(2,283)=11.6, p < 0.001 d = −0.61 d = −0.13
AWMA Block Recall Mean = 101.6
SD =12.7		 Mean = 98.6
SD =15.9		 F(2,160)=1.8, p=0.16 d = −0.21 d = 0.22
AWMA Listening Recall Mean = 111.7
SD = 16.2		 Mean = 107.2
SD = 18.3		 F(2,268)=3.9, p =0.04 d = −0.26 d = −0.06
AWMA Nonword Recall Mean = 108.5
SD = 11.2		 Mean = 90.8
SD = 15.9		 F(2,177)=32.1, p<0.001 d = −1.23 d = 0.18
AWMA Odd-One-Out Mean =116.1
SD = 15.9		 Mean = 110.2
SD = 16.9		 F(2,243)=3.1, p = 0.01 d = −0.36 d = 0.03
BRIEF Working Memory Mean = 50.2
SD =9		 Mean = 53.1
SD = 11.1		 F(2,252)=4.1, p =0.04 d = 0.28 d = 0.07
BRIEF Inhibit Mean = 49.9
SD = 8.6		 Mean = 52.3
SD = 10.8		 F(2,252)=1.6, p = 0.21 d = 0.23 d = 0.02
BRIEF Shift Mean = 49.2
SD = 10.1		 Mean = 50.8
SD = 9.9		 F(2,252)=1.5, p = 0.23 d = 0.16 d = 0.04
NEPSY Auditory Attention scaled score Mean = 9.7
SD = 2.8		 Mean = 9.1
SD = 3.9		 F(2,270)=1.5, p =0.23 d = −0.17 d = − 0.10
NEPSY Response Set scaled score Mean = 10.9
SD = 2.9		 Mean = 9.4
SD = 3.1		 F(2,270)=9.7, p=0.005 d=−0.44 d = 0.06
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CTH = Children with Typical Hearing; CHL = Children with hearing loss; WASI = Wechsler Abbreviated Scale of Intelligence; PPVT = Peabody Picture Vocabulary Test; CELF = Clinical Evaluation of Language Functioning; AWMA = Automated Working Memory Assessment; BRIEF = Behavior Rating Inventory of Executive Function. Group and sex difference are reported in Cohen’s d. Negative Cohen’s d values indicate lower scores for CHL (group) or Boys (sex).

For measures where significant differences were observed between children with typical hearing and CHH, the relative contributions of language abilities and audibility or auditory dosage on executive function skills for the CHH were assessed using Pearson correlations and linear regression models. Table 3 shows Pearson correlations between measures of auditory dosage, language, and executive function. Both aided audibility and auditory dosage were positively correlated with receptive vocabulary. Receptive vocabulary was also correlated with all measures of executive function with effect sizes ranging from small (r = 0.18 for NEPSY Response Set) to large (r = 0.58 for AWMA Listening Recall). Aided audibility was associated with AWMA Nonword Recall, but not any other measures of executive function. Auditory dosage was correlated with AWMA Nonword and NEPSY Response Set only.

Table 3 –

Pearson correlations between auditory measures, language, and executive function for children who are hard of hearing

Aided
SII		 Auditory
Dosage		 PPVT AWMA
Block		 AWMA
Nonword		 AWMA
Listening		 AWMA
Odd
One		 BRIEF
WM		 BRIEF
Inhibit		 BRIEF
Shift		 NEPSY
Auditory
Attention		 NEPSY
Response
Set		 WASI
Matrix		 WASI
Block
Aided SII 1 0.74 0.34 0.04 0.30 0.07 0.06 0.05 0.01 0.08 −0.04 0.12 −0.06 0.10
Auditory Dosage 1 0.31 −0.07 0.29 0.11 0.03 0.10 0.09 0.01 0.08 0.26 −0.02 0.08
PPVT 1 0.24 0.33 0.58 0.39 −0.33 −0.27 −0.29 0.27 0.18 0.39 0.34
AWMA Block 1 0.08 0.30 0.54 −0.21 −0.12 −0.11 0.27 0.29 0.42 0.22
AWMA Nonword 1 0.16 0.14 −0.12 −0.16 −0.09 0.01 0.01 0.07 0.04
AWMA Listening 1 0.41 −0.38 −0.31 −0.28 0.31 0.36 0.41 0.27
AWMA Odd One 1 −0.29 −0.10 −0.16 0.39 0.32 0.48 0.37
BRIEF WM 1 0.66 0.47 0.20 −0.23 −0.11 0.19
BRIEF Inhibit 1 0.15 0.04 −0.09 0.02 0.09
BRIEF Shift 1 −0.15 −0.14 −0.23 −0.22
NEPSY Auditory Attention 1 0.57 0.26 0.08
NEPSY Response Set 1 0.23 0.21
WASI Matrix 1 0.49
WASI Block 1
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Bold correlations were statistically significant at p < 0.05

PPVT = Peabody Picture Vocabulary Test; AWMA = Automated Working Memory Assessment; BRIEF WM Behavior Rating Inventory of Executive Function Working Memory Subscale.

To assess the multivariate relationship between language, audibility, auditory dosage, and executive function, linear regression models were conducted with receptive vocabulary (PPVT) and aided audibility for speech (aided SII) or auditory dosage as predictors of each measure of executive function. Table 4 summarizes the linear regression models. Figure 1 shows the relationship between receptive vocabulary and each measure of the AWMA, Figure 2 shows the relationship between receptive vocabulary and each subtest of the BRIEF, and Figure 3 shows the relationship between receptive vocabulary and the NEPSY subtests. For AWMA Listening Recall, AWMA Odd-One-Out, BRIEF Working Memory, and NEPSY Response Set, receptive vocabulary was a significant predictor of individual differences in executive function. Higher language abilities were associated with better executive function scores. Larger receptive vocabulary and greater auditory dosage both were associated with better nonword repetition scores on the AWMA Nonword Recall subtest and parent’s ratings of working memory and attention in everyday behavior on the BRIEF Working Memory subscale.

Table 4 –

Linear regression models with vocabulary and auditory dosage as predictors of executive function

Outcome Model Vocabulary (PPVT) Auditory dosage
AWMA Block Recall F(2,96) = 4.2, R 2 =0.08, p = 0.02 β= 0.29, p = 0.01 β= 0.05, p = 0.14
AWMA Nonword Recall F(2,106) = 10.4, R 2 =0.15, p < 0.001 β= 0.24, p = 0.01 β=0.92, p =0.007
AWMA Listening Recall F(2,268) = 28.2, R 2 =0.25, p <0.001 β= 0.55, p < 0.001 β=0.10, p =0.51
AWMA Odd-One-Out F(2,173) = 10.1, R 2 =0.13, p <0.001 β= 0.39, p <0.001 β=0.16, p =0.60
BRIEF Working Memory F(2,171) = 8.3, R 2 =0.15, p =0.003 β= − 0.17, p =0.009 β= − 0.19, p =0.001
BRIEF Inhibit F(2,171) = 2.2, R2=0.05, p =0.10 β= − 0.10, p =0.08 β= − 0.24, p =0.21
BRIEF Shift F(2,171) = 5.3, R 2 =0.08, p =0.005 β= − 0.13, p =0.003 β= − 0.2, p =0.26
NEPSY Auditory Attention F(2,190) = 4.7, R 2 =0.06, p =0.01 β= 0.05, p =0.008 β= − 0.02, p =0.48
NEPSY Response Set F(2,190) = 5.1, R 2 =0.09, p=0.008 β= 0.03, p = 0.02 β=0.05, p =0.23
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PPVT = Peabody Picture Vocabulary Test; AWMA = Automated Working Memory Assessment; BRIEF Behavior Rating Inventory of Executive Function.

Figure 1 –

Figure 1 –

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Automated Working Memory Assessment subtests standard scores by Peabody Picture Vocabulary Test standard score for children who are hard of hearing by Block Recall (A), Odd One Out (B), Nonword Repetition (C), and Listening Recall (D). Each circle represents an individual subject. The black solid line represents the best-fit to the linear relationship between variables.

Figure 2 –

Figure 2 –

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Behavior Rating Inventory for Executive Function subtests standard scores by Peabody Picture Vocabulary Test standard score for children who are hard of hearing by Working Memory (A), Inhibit (B), and Switch (C). Each circle represents an individual subject. The black solid line represents the best-fit to the linear relationship between variables.

Figure 3 –

Figure 3 –

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NEPSY-II subtests scaled scores by Peabody Picture Vocabulary Test standard score for children who are hard of hearing by Auditory Attention (A) and Response Set (B). Each circle represents an individual subject. The black solid line represents the best-fit to the linear relationship between variables.

Discussion

The goals of this study were to examine differences in language and executive function between children with typical hearing and CHH and to assess the relative contributions of auditory experience and language skills to executive function skills in CHH. Previous research has indicated that auditory experience and language are important for executive function in children who are deaf or who use cochlear implants, but the relative contributions of linguistic and auditory factors in CHH remained unclear. We found that CHH had deficits in language, working memory, and inhibition of attention, compared to children with typical hearing matched for age, socioeconomic status, and nonverbal intelligence. By assessing both auditory experience and language skills, we found that both factors supported executive function. Receptive vocabulary was broadly associated with nearly all measures of working memory and attention. Auditory dosage was associated with receptive vocabulary skills, verbal working memory, (Nonword Recall) and parent ratings of everyday working memory and attention behavior (BRIEF Working Memory subscale). Collectively, these results are consistent with previous studies that demonstrate the association between language abilities and executive function, but also support a direct association between verbal working memory and auditory experience after accounting for language.

The effects of hearing loss on language and executive function in CHH

As in previous studies, CHH demonstrated deficits in areas of language and executive function compared to children with typical hearing who were matched for age, socioeconomic status, and nonverbal intelligence. CHH had vocabulary scores that were nearly 2/3 of a standard deviation below their peers with typical hearing. This finding replicates previous studies that have demonstrated persistent language deficits for CHH, even for a group where most received the benefits of newborn hearing screening, early amplification, and early intervention (Tomblin et al. 2015; Nittrouer et al. 2017; Werfel 2017; Holt et al. 2020). CHH who had better audibility for speech and auditory experience, as indexed by a combination of their audibility for speech and amount of device use, had stronger receptive vocabulary, which is consistent with recent findings from this cohort related to device use (Walker et al. 2015), audibility (Tomblin et al. 2015; Walker et al. 2019; Tomblin et al. 2020), or a combination of both factors (Walker et al. 2020).

CHH also showed deficits compared to peers with typical hearing in areas of executive function related to working memory and attention. The finding of deficits in these areas of executive function is consistent with previous studies of children with cochlear implants (Pisoni & Cleary, 2003; AuBuchon et al. 2015; Nittrouer et al. 2017; Davidson et al. 2020) or hearing aids (Briscoe, Bishop, & Norbury, 2001; Willis et al. 2014, but also see Stiles et al. 2012). Differences between CHH and children with typical hearing were apparent from both verbal and visuospatial working memory tasks. The magnitude of statistically significant differences between CHH and peers with typical hearing for working memory tasks varied from small (d = 0.3 for AWMA Listening Recall) to large (d = 1.2 for AWMA Nonword Repetition). The only working memory task where CHH had comparable scores to children with typical hearing was the AWMA Block Recall subtest, which measures visuospatial short-term storage. The NEPSY Response Set scaled score was the only measure of attention that was significantly different between children with mild to severe hearing loss and peers with typical hearing. The NEPSY Response Set represents inhibition of attention and had a standardized mean difference between groups of approximately one-half standard deviation. The NEPSY Auditory Attention, BRIEF Inhibit, BRIEF Shift subtests were not significantly different between groups.

The mixed pattern of significant differences and range of effect sizes for working memory and attention highlight the heterogeneity in these skills for CHH. CHH showed greater variability than children with typical hearing for all measures of language and cognition, even when the group mean differences were small. The observation of individual variability in language, working memory, and attention among CHH in this study may help to explain the mixed pattern of findings in prior work that have relied on small sample sizes and group-level comparisons to children with typical hearing (Willis et al. 2014; Stiles et al. 2012). As a group, children who are deaf and have severe or profound degrees of hearing loss or use cochlear implants have shown larger deficits in working memory and attention compared to children with typical hearing than CHH (Pisoni & Cleary, 2003; Davidson et al. 2020). Our findings support this speculation as differences in auditory experience and language were associated with executive function for CHH even when CHH did not have poorer scores than children with typical hearing at the group level. Examining the effects of variability in auditory dosage and language skills on working memory and attention in CHH as we did in this study may help to better characterize which CHH are at risk for delays in executive function than group-level comparisons to children with typical hearing.

Predictors of language and executive function in children with hearing loss

The association between language and executive function was also examined. Language was associated with all measures of working memory and attention. Auditory dosage was associated with receptive vocabulary. After controlling for receptive vocabulary, auditory dosage was only related to short-term verbal working memory, measured by the AWMA Nonword Repetition subtest. Auditory dosage was also associated with inhibition of attention as measured by the NEPSY Response Set subtest after controlling for receptive vocabulary. The NEPSY Response Set subtest was also significantly poorer in CHH than in peers with typical hearing, suggesting that this measure of inhibition of attention may be particularly sensitive to differences in auditory dosage.

This pattern of relationships between audibility, language, and executive function skills for CHH is consistent with previous literature on children who are deaf or who use cochlear implants (Dye & Hauser, 2014; Hall et al. 2018a; Conway et al. 2009; Kronenberger et al. 2013; Nittrouer et al. 2017; Botting et al. 2017). Jones and colleagues (2020) found that early language abilities predicted later executive function skills in children with mild to profound hearing loss, but variation in auditory experience was not examined for that group. Auditory experience is widely known to influence language development in children with hearing loss whether examined as audiometric pure-tone average (Ching et al. 2013; Sininger et al. 2013), audibility for speech (Tomblin et al. 2015), or characterized as auditory dosage using a combination of speech audibility and hearing aid use (Walker et al. 2020). We confirmed the relationship between auditory experience and language, as children with hearing loss who had greater auditory dosage had stronger receptive vocabulary abilities. This pattern of findings is consistent with more recent systems-based theories of executive function of children who are deaf or use cochlear implants that suggest that a complex interplay between auditory experience, language, and executive function may help to explain deficits in executive function for CHH (Hall, 2020). The Intersubjectivity Scaffolding Hypothesis (Morgan & Dye, 2020) focuses on the interactions between children and their communication partners that foster early development of executive function and provide support for the development of more complex language skills over time. This account is consistent with our previous research with this cohort examining the importance of parental responsive to language development (Ambrose et al. 2015). The role of auditory dosage in supporting these parent-child interactions has not been studied, but the current study results suggest that children with higher auditory dosage may have advantages in terms of language and some areas of executive function that scaffold these early interactions. The cross-sectional analysis approach used here cannot be used to infer the direction or causality of the relationships between auditory, linguistic, and cognitive variables for CHH, but underscores the importance of both auditory experience and language skills for executive function in this population.

For executive function tasks that are closely linked with language processing, such as verbal working memory, the associations reported in this study are intuitive and fit with the larger literature on mechanisms for language development. Language abilities support verbal working memory tasks by allowing for encoding of serial phonological information (Gathercole & Baddeley, 2014). Deficits in verbal working memory have been associated with developmental language disorders (Montgomery et al. 2010) and with phonological awareness and vocabulary skills in children who use cochlear implants (Nittrouer et al. 2017). Thus, the relationship between verbal working memory and language outcomes among children with hearing loss are not surprising.

The mechanism for the association between attention and visuospatial measures of working memory is less straightforward, but also has been documented in the extant literature. Deficits in visuospatial working memory and attention among children who are deaf have been interpreted as evidence for domain general effects of auditory experience on specific areas of executive function (Conway et al. 2009). Language is often recognized as important for processes related to self-talk and emotional regulation in children (e.g., Cole, Armstrong, & Pemberton, 2010). The relationship between language and non-verbal domains of executive function also could be related to the use of verbal rehearsal strategies for non-verbal working memory tasks. AuBuchon and colleagues (2015) found differences in forward and backward digit span between children with typical hearing and children with cochlear implants even when the digits were presented visually and using a non-verbal pointing response. Receptive vocabulary was correlated with digit span across auditory and visual conditions, leading the authors to conclude that deficits in working memory tasks are likely related to a combination of poor phonological and lexical representations in long term memory that limit reactivation during working memory tasks. Pisoni and colleagues (2011) have also suggested that sequences used for visuospatial working memory tasks in previous studies may have features, include color and shape, which can be used by children to verbally encode these sequences using verbal labels. The observation of relationships between auditory dosage and nonverbal measures of executive function is also consistent with the predictions of the Biopsychosocial Systems Theories of executive function. These theoretical accounts posit that auditory experience, language, and executive function are interactive during early childhood and reflect a broad range of factors including genetics, sensory experiences, and the family environment. Whereas auditory dosage is conceptualized as a combination of hearing aid fitting quality and hearing aid use, individual differences in auditory dosage are likely the result of a combination of complex factors including each child’s degree of hearing loss, access to quality audiological services, and family environment. The current analysis relied mostly on laboratory measures of language and executive function, but the positive relationships between auditory dosage, language and the BRIEF working memory subscale support that these effects extend in the child’s real-world environment. The BRIEF working memory subscale assesses the parent’s perceptions of working memory function in the child’s real world environment, and the observation that auditory dosage and language were related to this scale is consistent with Biopsychosocial Systems Theories and recent evidence that the family environment has an important influence on executive function in children who are deaf or hard of hearing (Holt et al. 2020; Blank et al. 2021). Likewise, language and executive function skills were associated with measures of nonverbal intelligence, supporting the role of general neurocognitive factors in these complex relationships for CHH and consistent with systems-based theoretical models. These findings highlight the interdependence of language and executive function skills in children is highlighted and is consistent with the associations observed in the current study.

Clinical implications

The results of this study highlight several malleable factors that could be targeted for intervention to improve language and executive function skills in children with hearing loss. The finding that auditory dosage predicts receptive vocabulary abilities and some aspects of verbal working memory supports the idea that children with hearing loss whose parents want them to develop spoken language should be identified with hearing loss, fitted with amplification (if appropriate), and enrolled in early intervention at the earliest possible age. Early intervention for children with hearing loss already targets promoting access to language at an early age and those strategies are likely to also benefit other areas of executive function, particularly working memory. A two-pronged approach of providing auditory and linguistic access for children with hearing loss would appear to provide a direct benefit for executive function for children whose parents choose spoken language as a communication modality. Importantly, the children with hearing loss in this study continued to show language deficits compared to peers with typical hearing with access to many of the interventions described above. Even when children with hearing loss are fitted with hearing aids at an early age, recent data suggests that the speech audibility provided by those fitting varies considerably and is often less than what is prescribed to increase speech audibility (McCreery et al. 2015). As a result, not all children with hearing aids experience optimal access to language through their devices. Audiologists can have an impact on the audibility of the fitting by using validated prescriptive targets for children (Moodie et al. 2019). Strategies for increasing hearing aid use have also been developed and could further increase the auditory dosage of children with hearing loss (Ambrose et al. 2020). Evidence also suggests that children who are deaf who have access sign language achieve comparable executive function skills to children with typical hearing (e.g. Dye & Hauser, 2014), suggesting that the provision of visual language could be an alternative intervention strategy to support the development of executive function. The potential for sign language as an intervention strategy for children with mild to severe degrees of hearing loss who have more residual hearing has not been directly evaluated in previous studies to our knowledge.

Limitations and future directions

Although this study examined the associations between auditory, linguistic, and cognitive skills in a large group of children with mild to severe hearing loss, there are several limitations of the current study that should be considered. The sample of children with hearing loss in the current study have demographic characteristics that differ from the general population of children with hearing loss in the United States. Children from non-English speaking homes were excluded due to the use of measures that are standardized in spoken English. Children who had additional developmental comorbidities were excluded from the sample to avoid confounds related to interpretation of deficits in executive function related to other developmental conditions. Although the children with hearing loss were matched with children with typical hearing on measures of nonverbal intelligence and maternal educational level, both groups had higher levels of maternal education than the general population. This combination of sample characteristics means that the language and executive function skills of this sample are likely to be better than the general population of children with hearing loss. Inclusion of a more diverse sample would have increased variability across all the outcome measures and could allow broader generalization of these results.

The associations between auditory dosage, language, and executive function skills also support directions for future research. The current study relied on standardized measures of language ability, but functional measures of auditory and language development, often assessed using parent or teacher questionnaires, may provide a broader picture of the child’s functioning in their home and educational environments. The relationship between these functional measures, auditory dosage, and executive function could provide novel insights about the relationships between these constructs. The cross-sectional approach used in the current study does not characterize the growth trajectories of executive function skills in CHH over time. Longitudinal studies can lead to stronger interpretation of the relationships between auditory dosage, language, and executive function, as in previous studies of language and executive function for children who are deaf and CHH (e.g., Jones et al. 2020). Executive function also continues to develop through adolescence, and both longitudinal and cross-sectional studies are needed to better characterize the long-term impact of deficits in executive function for CHH in early primary school years on executive function, behavior, and academic performance in adolescence. Additionally, neuroimaging studies may help to associate the behavioral differences observed in this study with structural and functional changes in the brains of CHH that could be used as biomarkers for assessing the benefits of early intervention and treatment.

Conclusions

The current study sought to examine the relationships between measures of auditory experience, language, and executive function. Using a large sample of CHH and children who typical hearing matched for age, nonverbal intelligence, and socioeconomic status, we found that CHH had deficits in language, working memory, and inhibition of attention. These deficits were associated with individual differences in language after controlling for auditory experience, measured as auditory dosage. Individual differences in auditory experience were associated with verbal working memory and attention after controlling for the influence of language. These results call attention to the complex inter-relationships between auditory, linguistic, and cognitive development consistent with systems-based theories of executive function and provide motivation for future research. Intervention approaches that attempt to maximize auditory and language access could support executive function skills in children with mild to severe hearing loss and should be examined in future research.

Acknowledgements

This work was supported by grants from the NIH/NIDCD R01DC013594 and R01DC009560 and NIGMS P30 DC004662. The content of this project is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute on Deafness and Other Communication Disorders or the National Institutes of Health. The authors would like to thank Angela AuBuchon for comments on a draft of this manuscript. Special thanks go to the examiners at the University of Iowa, Boys Town National Research Hospital and University of North Carolina-Chapel Hill and the families and children who participated in the research.

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