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Cognitive skills in children with Usher syndrome type 1 and cochlear implants
International Journal of Pediatric Otorhinolaryngology 76 (2012) 1449–1457
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Cognitive skills in children with Usher syndrome type 1 and cochlear implants Cecilia Henricson a,b,d,*, Malin Wass a,b,d, Bjo¨rn Lidestam b,d, Claes Mo¨ller a,b,c, Bjo¨rn Lyxell a,b,d a
Swedish Institute for Disability Research (SIDR), Sweden Linnaeus Centre for Research on Hearing and Deafness (HEAD), Sweden c Audiological Research Centre, O¨rebro University Hospital, O¨rebro University, Sweden d Department of Behavioral Sciences and Learning, Linko¨ping University, Linko¨ping, Sweden b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 22 March 2012 Received in revised form 30 May 2012 Accepted 3 June 2012 Available online 12 July 2012
Introduction: Usher syndrome is a genetic condition causing deaf-blindness and is one of the most common causes of syndromic deafness. Individuals with USH1 in Sweden born during the last 15 years have typically received cochlear implants (CI) as treatment for their congenital, profound hearing loss. Recent research in genetics indicates that the cause of deafness in individuals with Usher type 1 (USH1) could be beneficial for the outcome with cochlear implants (CI). This population has not previously been the focus of cognitive research. Objective: The present study aims to examine the phonological and lexical skills and working memory capacity (WMC) in children with USH1 and CI and to compare their performance with children with NH, children with hearing-impairment using hearing-aids and to children with non-USH1 deafness using CI. The participants were 7 children aged 7–16 years with USH1 and CI. Methods: The participants performed 10 sets of tasks measuring phonological and lexical skills and working memory capacity. Conclusions: The results indicate that children with USH1 and CI as a group in general have a similar level of performance on the cognitive tasks as children with hearing impairment and hearing aids. The group with USH1 and CI has a different performance profile on the tests of working memory, phonological skill and lexical skill than children with non-USH1 deafness using CI, on tasks of phonological working memory and phonological skill. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Children with cochlear implants Usher syndrome type 1 Spoken language Cognition Phonological skills Lexical skills Working memory
1. Introduction Usher syndrome (USH) is a genetic condition affecting hearing, balance and vision with a prevalence of 3.0–3.6/100,000 newborns in Sweden [1,2]. It is one of the most common causes of syndromic deafness [2,3], and there are three different clinical types (types 1–3) [1,2,4]. Usher type 1 (USH1) has a congenital, profound bilateral deafness, lack of bilateral vestibular function (areflexia) and retinitis pigmentosa (RP), causing degeneration of the rods of the retina, with impaired night vision, progressive narrowing of visual field and loss of peripheral vision as a result [2,4]. Most individuals with Usher syndrome have remaining central vision of 5–108 in late adulthood [2,4]. Type 2 displays a congenital, moderate to severe hearing loss which remains rather stable through life, RP, and normal vestibular function [2,4].
* Corresponding author at: Department of Behavioral Sciences and Learning, Linko¨pings Universitet, S-582 35 Linko¨ping, Sweden. Tel.: +46 13 28 20 91; fax: +46 13 28 21 45. E-mail address: [email protected] (C. Henricson). 0165-5876/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2012.06.020
Usher syndrome type 3 can display both pre- and post-lingual onsets of progressive moderate to severe hearing loss, as well as progressive loss of vestibular function and occasionally late onset of RP [2]. In the present study, focus is on children with USH1. The prevalence of congenital, syndromic and non-syndromic, deafness in Sweden is about 1–2/1000 newborns [5] and the vast majority of children (including children with USH1) are treated with cochlear implantation (CI), performed within the first two years of age. CI is an implantable biomedical device providing auditory sensation to individuals with profound sensori-neural hearing loss [6]. The outer parts consist of a microphone, a signal processor and (radio) transmitter. The implanted parts are a combined receiver and transmitter, placed beneath the skin in the bone of the back of the skull, as well as an array of electrodes that has been inserted into the coil of the inner ear. The cochlear implant converts the incoming sounds to electrical pulses which are transmitted through the electrodes [6]. There is an accumulating body of knowledge regarding the development of speech, language and cognitive skills in deaf and hearing-impaired children with CI [e.g. 7–9,6,10–12]. The findings indicate that the development of spoken language
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skills in the majority of children with CI is adequate to allow for verbal communication to be the primary mode of communication, and that these skills are likely to be more complex and better developed the earlier the implantation is done [8,9,6,10,11]. Previous research has not focused on development of speech, language and cognitive skills in the population of children with USH1 and our level of knowledge is thus limited with respect to their cognitive development. Exploring aspects of cognition related to hearing and language in this group has another caveat as well. Children who receive cochlear implants are typically regarded as one population in research and rehabilitation, and this study represents an attempt to explore whether this assumption is valid. In the present study, focus is on working memory (WM) and phonological and lexical skills. These cognitive abilities are important for the development of complex and composite skills such as communication and reading [13]. The concept of working memory refers to the simultaneous storage and processing of information [14]. Working memory is a theoretical construct implying a continuous on-line ability, used in almost all everyday situations [13–16]. It is a memory system that includes four components: a central executive, a visual loop, a phonological loop and an episodic buffer [14]. The central executive is responsible for planning, co-ordination and execution of activities within the working memory system. The phonological loop is responsible for manipulation, storage and processing of auditory information. The visual loop serves a similar purpose for visual or spatial information. The episodic buffer is a link between new, incoming information and old information stored in long-term memory. The phonological loop is a subsystem in WM that simultaneously stores and processes auditory input, for example speech sounds [i.e. 16]. Phonological WM is important in particular during vocabulary development [13,16] and Wass et al. [17] found that children with CI had significantly poorer phonological WM than children with normal hearing, corroborating other studies on spoken language skills in children with CI [e.g. 11,18]. However, it is important to note that in the study by Wass et al. [17] there was only a small significance for the difference between the groups on general WM, indicating that some children with CI reach the same level of development of general WM as children with NH, and there was no difference between the groups regarding visual WM. Phonological skills are important for language development [9,6,19,20]. Phonological skill is an umbrella term implying the processing and decision-making about phonological information [17]. The process of finding and retrieving verbal labels from long term memory (i.e. matching incoming speech stimuli to the correct word and its meaning) is termed lexical access, and this cognitive ability correlates with phonological skill and phonological WM [17]. Wass et al. [17] found that children with cochlear implants display significantly poorer phonological skills and lexical access than children with NH. Most of the phonological skills and lexical access are fully developed by age 5–6 in children with NH and typical language development [e.g. 16,17,19].
The aim of this study was to examine the level of development of phonological and lexical skills, and working memory capacity (WMC), in a population of children with Usher type I using CI. The performance of this group was compared to that of children with normal hearing (NH), to children with hearing-impairment using hearing-aids, and to children with non-USH1 deafness using CI.
2. Material and methods The participants were recruited from a register at the ¨ rebro, Audiological Research Centre, University Hospital of O Sweden and from the family organization for children with CI in Sweden, Barnplantorna. The study was approved by the regional ¨ rebro. Care-giver informed consent ethic committee of Uppsala-O in written form was received from all the participants. A letter of information directed to the children was also included in the information about the study given to the care-givers of the participants. 2.1. Participants Inclusion criteria for the group with USH1 were (1) a confirmed diagnosis of USH1, (2) age between 6 and 16 years, (3) no known (except for visual) co-existing disability, (4) performance within, or above, their age norm on block design from WISC-III, and (5) Swedish as the primary language and no known language impairment. The diagnosis of USH1 had been set clinically and genetically. Of the seven participants, 2 had USH1b, and 3 had USH1d. For two participants there was not yet a confirmed genetic diagnosis. No visual data on the participants were available for this study, but according to information from parents and participants, the visual problems were not yet large enough to interrupt performance at situations such as those experienced during testing. Regarding the control group with CI inclusion criteria were (1) a diagnosis or cause of profound deafness other than Usher syndrome, (2) age between 6 and 14 years (3) no known coexisting disability, (4) performance within, or above, their age norm on block design from WISC-III, and (5) Swedish as the primary language and no known language impairment. The 33 children in the control group with CI had diagnoses as follows: 20 had unspecified congenital deafness, 6 had unspecified congenital and progressive severe hearing loss, 3 had acquired deafness due to CMV-infection, 2 had LVAS, 1 had PN Meningitis, 1 had Wardenbu syndrome and 1 had Mondini malformation. The control group with hearing impairment using hearing aids had similar inclusion criteria as the control group with CI, though the first criteria was a confirmed hearing loss requiring hearing aid. For the control group with normal hearing the inclusion criteria were (1) no known existing hearing problems and no ear infections during the last three months, (2) age between 6 and 12 years, and (3) Swedish as the primary language and no known language impairment. The highest age for inclusion is lower for this group than the others,
Table 1 Demographics of the participants with Usher syndrome type 1. Participant
Age (y.:mo.)
Age at 1st CI
Age at 2nd CI
Language
Bilateral
1 2 3 4 5 6 7
7:6 8:0 8:1 8:10 12:4 12:11 15:11
20 months 18 months 12 months 9.5 months 39 months 32 months 4 years
22 months 30 months 30 months 18 months – 8.5 years 12 years
Spoken Sw. Spoken Sw. Spoken Sw. Spoken Sw. Sign supported Sw. Spoken Sw. SSL/spoken Sw.
Yes Yes Yes Yes No Yes Yes
Sw., Swedish; SSL, Swedish sign language.
C. Henricson et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1449–1457 Table 2 Description of the groups using CI.
Age at diagnosis (y.:mo.) n Mean SD Range Age at 1st CI (y.:mo.) n Mean SD Range Age at 2nd CI (y.:mo.) n Mean SD Range Age at testing (y.:mo.) n Mean SD Range
USH1
Control group CI
7 1:1 0:10 1:11
33 1:2 0:10 3:0
7 1:1 1:2 3:2
33 3:6 2:0 8:1
6 4:8 4:3 10:6
21 6:11 1:8 6:10
7 10:3 3:0 8:5
33 8:11 2:0 7:9
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language pathologists for percent consonants correctly reproduced (pcc). The scoring was done in the same way for the repeated items in Serial Recall of Non-words but the task in this test was for the participant to repeat back increasing series of one-syllable non-words. Complex span (i.e. simultaneous storing and processing of information) was measured by Sentence Completion and Recall [21]. The participants listened to series of 2–5 incomplete sentences and were asked to fill in the last word (e.g. ‘‘Tomatoes are red, crocodiles are. . .’’) and memorize it for later recall, the result of the test being number of correctly recalled words. Visuo-spatial working memory was measured by the Visual Matrix Pattern test [17], in which a 5 5 matrix of grey colored cells is displayed. A set number of cells switch simultaneously to black color, starting at 1 and increasing every third trial up to a maximum of 8 cells, and disappear after short display. The participant is then asked to click the cells which were previously black. The score is the highest number of cells successfully identified by the participant at two of the three trials. 2.4. Phonological skills
since piloting of the tests showed ceiling effects for children with normal hearing above age 12. The groups consist of (1) 7 children with USH1, (2) 33 children with non-USH1 deafness using CI, (3) 43 children with hearing impairment (HI) using hearing aids (HA) and (4) 120 children with NH. For group 3, the mean age at testing was 9 years and 3 months (SD = 1 y. 9 mo.) and for group 4 mean age at testing was 9 years and 2 months (SD = 1 y. 8 mo.). The demographics of the children with USH1 and CI are displayed in Table 1. See Table 2 for information about the two groups with CI regarding ages at diagnosis, implantation and testing. 2.2. Methods The participants were tested at the Audiological Research ¨ rebro, in their school setting, or in their home. The test Centre in O block-design from WISC-III was used to ascertain that the cognitive performance of the participating children was within the norm with respect to their age group. The tests were administered on a lap-top computer and consisted of a test battery designed to measure phonological skills, lexical skills, phonological WM, complex WM and visuospatial WM, called the Sound Information Processing Systems (SIPS) [17]. All of the tests in SIPS, except for a measure of visual WM and one of passive naming, were presented in auditory-only in the same female speaker voice. The auditory stimuli were presented with loudspeakers (Logitech S-100) which were set by the child to a level of comfortable loudness [cf. 8,17]. Short descriptions of each category of tests are given here. An extensive description of the tests and procedures is given in Wass et al. [17].
Phonological skills were measured by three tests, each designed to measure different aspects of phonological skills. The tests used were: Non-word Discrimination, Phonological Representations, and Phoneme Identification [17]. The task in Non-word Discrimination was for the participant to press a button if the presented pair out of 16 non-words were identical. In order to achieve maximum score (8) on the test, the participant had to discriminate correctly for all pairs, same and different (i.e. push when identical and not push button when pairs were different). Real words were used in the test Phonological Representations in which the participant is asked to report on when a familiar word is pronounced correctly out of several options. To make certain that the participant was familiar with the word s/he was shown an illustration of the word (i.e. ‘‘sofa’’) and asked to say what was depicted. The task in Phoneme Identification was to press a button if there was a specific language sound within the auditorily presented non-words (i.e. ‘‘is there ‘r’ in ‘federur’?’’ or ‘‘is there ‘s’ in ‘ho¨ntpule’?’’). 2.5. Lexical access This ability was measured by three tests: Word-spotting, Semantic Decision Making and Word Mobilization. In word-spotting the participant was asked to push a button as soon as s/he identified a real word among series of one syllable non-words. Semantic Decision Making required the participant to push a button when there was a word adhering to a specific, defined category (i.e. ‘‘push the button when you hear something that is an animal’’) and hence uses real words as stimuli. Word Mobilization also used real words and the task was to identify the matching picture among four alternatives after a word had been presented. 2.6. Statistics
2.3. Working memory The tasks designed to measure WM were all presented in auditory only, except for Visual Matrix Pattern test. Phonological WM was measured by Non-word Repetition and by Serial Recall of one-syllable non-words. In order to ensure that the results were not affected by vocabulary or word knowledge (or both combined), non-words were used as stimuli in these two sets of tasks tapping phonological WM. In the test Non-word Repetition, the participant is asked to repeat back non-words of increasing syllable length. The repetition attempts were recorded at the test-occasion and scored off-line by speech and
The results from the present study were computed in two different ways. First, the confidence intervals of the groups on a 0.05 significance level (CI95) were calculated and compared in order to establish possible group differences for mean performance. Secondly, the pattern of performance among the individuals with USH1 is described in relation to linear models of the mean values of the control groups (i.e. regression lines). The performance in the different tasks is in these analyses described as a function of age, as the variation of performance across age is different in the group with USH1 and for control groups. The performance of the children with USH1 is presented in Figs. 1–3.
[(Fig._1)TD$IG]
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Fig. 1. Results on measures of working memory in relation to age in months. The individuals’ values in the three control groups are displayed. Linear regression models of the control groups’ means are displayed, with confidence intervals (CI95) of the model. The individual performances of the participants with Usher syndrome type 1 are shown in each panel, each participant with a unique number (1–7).
[(Fig._2)TD$IG]
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Fig. 2. Results on measures of lexical skill in relation to age in months. The individuals’ values in the three control groups are displayed. Linear regression models of the control groups’ means are displayed, with confidence intervals (CI95) of the model. The individual performances of the participants with Usher syndrome type 1 are shown in each panel, each participant with a unique number (1–7).
3.1. Comparisons of group means
group with CI. No significant differences were obtained between the USH1 group and the groups of children with HI, and children with NH on this task. For the two phonological working-memory tasks, the children with NH scored significantly higher than all the other three groups. No significant difference in performance emerged between the children with USH1, the control group with CI, and the children with hearing-impairment, on the tasks measuring phonological WM. For the visual working memory task, performance was similar between the USH1 group and the three other groups.
3.1.1. Working memory capacity The children with USH1 scored significantly higher on general WM (Sentence Completion and Recall), than the control
3.1.2. Lexical skills The children with USH1 scored significantly higher than the control group with CI on one of three lexical tasks
3. Results The results will be presented in two parts. First, the means for the groups, and the statistically significant differences of the means between the group with USH1 and the control groups will be presented (see Table 3). This is followed by an account of the performance of the individuals with USH1 in relation to the control groups (see Figs. 1–3).
[(Fig._3)TD$IG]
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Fig. 3. Results on measures of phonological skill in relation to age in months. The individuals’ values in the three control groups are displayed. Linear regression models of the control groups’ means are displayed, with confidence intervals (CI95) of the model. The individual performances of the participants with Usher syndrome type 1 are shown in each panel, each participant with a unique number (1–7).
(Word Mobilization). No other differences between the group with USH1 and the three control groups proved to be significant on these tasks. 3.1.3. Phonological skills The children with USH1 scored significantly higher than the control group with CI on the Non-Word Discrimination task, while no significant difference was found between the children with USH1 and the children with NH or HI. No significant difference was found in the Phoneme Identification task or the task Phonological Representations between the USH1 group and the other groups. However, it should be noted that the both
groups of deaf children with CI scored significantly lower on these tasks compared to the NH group. 3.2. Performance of the individuals with USH1 in relation to control groups and age The performance of the participants with USH1 is presented as number of individuals in the group performing above, on or below the 95% confidence bands of the control group’s regression lines. Results are displayed in Figs. 1–3. Each panel of a figure displays the performance of the individuals from a specific control group, as well as the regression line with CI95 for that group. The
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Table 3 Mean values and confidence intervals of the groups, and number of participants in each group on every measure. Working memory
USH1 NH HI using HA Deaf CI
Visual Matrix Pattern
Sentence Completion and Recall
Serial Recall of Non-words (pcc)
Non-word Repetition (pcc)
n
M (CI95)
n
M (CI95)
n
M (CI95)
n
M (CI95)
7 120 43 33
5.0 4.7 4.4 3.9
7 120 43 28
12.7 (10.7–14.7) 12.3 (11.9–12.8) 12.0 (11.3–12.8) 8.4 (6.9–10.0)
7 116 43 26
33.6 57.9 45.7 28.2
7 117 43 26
58.1 88.2 76.5 39.0
(3.3–6.6) (4.4–4.9) (4.0–4.8) (3.4–4.5)
(16.5–50.7) (55.8–60.1) (41.7–49.7) (25.2–33.3)
(41.6–74.6) (86.9–89.5) (73.1–80.0) (32.0–45.8)
Lexical skills Word Mobilization
USH1 NH HI using HA Deaf CI
Word-spotting
Semantic Decision Making
n
M (CI95)
n
M (CI95)
n
M (CI95)
6 120 43 38
7.8 8.7 8.5 5.9
4 120 43 31
4.8 7.9 6.3 3.7
7 120 43 36
22.9 28.3 28.3 24.8
(6.6–9.1) (8.6–8.8) (8.3–8.8) (5.1–6.6)
(1.0–8.5) (7.7–8.1) (5.7–6.9) (2.96–4.5)
(17.5–28.2) (28.1–28.5) (28.0–28.6) (23.5–26.1)
Phonological skills
USH1 NH HI using HA Deaf CI
Phonological Representations
Non-word Discrimination
Phoneme Identification
n
M (CI95)
n
M (CI95)
n
M (CI95)
5 46 43 15
15.8 17.9 17.3 15.5
6 120 43 28
7.2 7.9 7.1 4.8
5 46 43 13
8.8 (5.1–12.5) 11.4 (11.2–11.7) 11.7 (8.6–14.8) 7 (4.9–9.1)
(11.9–19.7) (17.9–18.0) (17.1–17.5) (14.2–16.9)
(6.1–8.2) (7.8–7.9) (6.7–7.5) (3.9–5.6)
performance of each child with USH1 and CI is superimposed on the performance of the control groups.
and to the control group with CI on another set of tasks (see Fig. 3, phonological skill).
3.2.1. Working memory The majority of the participants with USH1 perform similar to children with HI using HA, and children with NH of the same age, on the tasks measuring general WM (Fig. 1, general WM). Regarding visual WM the range of performance among the children with USH1 is wider, with the performance of one participant exceeding, and two participants performing below, the three control groups (Fig. 1, visual WM). The results from the two sets of tasks measuring phonological WM showed that the children with USH1 in general had higher performance than the control group with CI on Non-word Repetition, while the two groups with CI had similar performance on Serial Recall of Nonwords (Fig. 1, phonological WM). Only two of the participants with USH1 had performance above, and similar to, that of children with NH or HI using HA, while the other five performed below these groups (Fig. 1, phonological WM).
4. Discussion
3.2.2. Lexical skill The results showed a high degree of variation in performance among and within the participants with USH1 on the tasks measuring lexical skill. One participant had performance similar to that of children with NH and children with HI using HA, on two out of three sets of tasks. Several of the participants displayed higher performance than the control group with CI on two of the tasks measuring lexical skill (see Fig. 2, lexical skill, Word Mobilization and Semantic Decision Making). 3.2.3. Phonological skill The results display that two individuals with USH1 had consistently higher scores than the control group with CI, and a performance similar to that of the control group with HI using HA (see Fig. 3, phonological skill). The other participants with USH1 varied in performance on the different sets of tasks, performing similar to the control groups with NH or HI using HA on some tasks
The present study examined working memory capacity, phonological and lexical skills in children with USH1 and CI. The performance of 7 children with USH1 and CI was related to populations of children with normal hearing, to children with hearing impairment using hearing aids and to children with nonUSH1 deafness using CI. In sum, the general pattern of results showed that, as a group, the children with USH1 have performance levels on the cognitive tests used in the study that do not differ significantly from the control group of children with NH, except for specific abilities such as phonological working memory. The control group with NH had, as expected, significantly higher results on phonological working memory than the three other groups (see [7,17] for similar results). Though there is a high variation in performance among the children with USH1, they receive higher scores on specific aspects of phonological WM and phonological skill than the control group of children with CI. Working memory capacity, lexical and phonological skills are abilities that develop and refine during childhood [13,21], thus, it was important to examine developmental trends in the control groups in order to see how the individuals with USH1 and CI performs with respect to their chronological age. Most of the participants with USH1 displayed a performance level on general, and visual, working memory tasks that is similar to that of children with NH and to children with HI using HA of the same age. However, the results of the children with USH1 could seem contradictory, since they outperform the group of children with non-syndromic deafness and CI on one measure but perform similar, poor results on the other. The two tasks of phonological working memory differ such that in the Non-word Repetition tasks the non-words have a complex syllable structure and contain supra-segmental properties (i.e. stress patterns and intonations [17,20,22]) whereas
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in Serial Recall of Non-words the non-words are of simple CVCstructure [17,20,22]. In Serial Recall of Non-words the majority of individuals with USH1 perform similarly to the control group with CI, while six out of the seven children with USH1 perform higher scores on Non-word Repetition. This may indicate that the children with USH1 are able to make more use of the suprasegmental properties than the deaf children with CI. The results also display that the children with USH1 who have had early implantation (participants 1–4; age at implantation < 2 years) tended to perform in line with the expected performance level for children with HI using HA, or even in some cases as children with NH, of the same age. This level of performance is in contrast to the children with USH1 who received implants at later ages (participants 5–7). The children with later implantation tended to perform similar to other deaf children with CI of the same age on tasks assessing phonological working memory and phonological skill. These findings corroborate previous research [17,23] that noted a lag in the development of phonological and lexical skills, particularly for children with late implantation (age > 3). Similarly, Sharma et al. [24], using an ERP-paradigm, found that the brain responses to speech sounds were deviant in children with this late implantation in comparison to children with early implantation, whose brain response was similar to that of children with NH (see also Kral and Sharma [25]). Similar to previous research [6,7,9], this may indicate an atypical development of phonological working memory and phonological skills in children with late implantation. An atypical development of these abilities and skills could influence the development of composite skills such as reading [17]. Lack of auditory stimulation, as well as a less detailed signal from the cochlear implant, is generally suggested as parts of the explanation to the deviant development of spoken language skills in individuals with CI [e.g. 6,12,23,26]. However, one main finding of the present study is that the participants with USH1 have better developed phonological and lexical skill, and that one aspect of phonological working memory appears to be more capacious in the children with USH1 than in the control group of CI-users. The performance of the group with USH1 was actually more similar to that of children with HI using HA than to other deaf children with CI across most tasks. These findings could be indications of individuals with USH1 having different prerequisites for hearing with CI, than individuals with other types of deafness. Recent research on animal models with Usher syndrome has revealed the phenotypic expression and functional consequences of the mutated genes causing USH1 [e.g. 27–30]. The results indicate a disruption in the function of the stereocilia of the IHC in the cochlea, causing the profound hearing loss [30]. In for example GJB2 (Connexin 26), a nonsyndromic cause of deafness, the mutations seem to primarily affect the cell bodies of the IHC, and aspects of the membranes separating the Scala media from the Scala tympani [31]. If there are remaining IHC in humans with USH1, these could be important in the functioning with a cochlear implant (CI). It is thought that a CI in typical cases stimulates the spiral ganglion cells. There is a possibility that the CI not only stimulates the spiral ganglion cells, but also that the IHCs interact with the electrical stimulation, i.e. by flexing and firing neural pulses, thus, allowing for more nuanced auditory stimulation than other deaf individuals using CI have. A more detailed auditory signal would, in turn, be beneficial for the development of cognitive skills associated with hearing [17,32]. Following this, the higher performance of the group with USH1 on tasks of phonological working memory and phonological and lexical skills compared to the control group of CI-users could be explained. The children with USH1 participating in this study are also likely to benefit from the fact that they have received an early
diagnosis, which means that there are early interventions and awareness of that these individuals will lose vision and thus will become increasingly dependent on their CIs. This awareness could trigger great efforts to build the children’s competence in using their implants, which in addition to a potentially more detailed auditory signal would benefit these children’s development of the cognitive abilities associated with hearing. The idea of existing but non-operational inner hair cells in humans with USH1 is intriguing, and hopefully future research projects will explore the findings of the present study and what reasons there could be to the group differences. More profound knowledge regarding the morphology and the physiology of OHC and IHC in Usher syndrome is also needed. Given the small sample of participants with USH1 in this study, more research is needed in order to validate and replicate the findings. However, the seven participants comprise a fairly large proportion of the Swedish population with USH1 in the age of 6–16 years, and thus the findings are interesting despite the limitation of the small sample size. Also, the data has been analyzed on two levels, group and individual, and both analyses converge to the same pattern; the participants with USH1 perform better on specific tasks than their peers with CI. This could be claimed to further validate the findings. In conclusion, the findings of the present study indicate that some aspects of phonological WM and phonological skill are better developed in the participants with USH1. This could be an indication of prerequisites for developing more defined phonological skills than other deaf children with CI. It could also be the result of more focused interventions due to the fact that the children and their environment in an early stage are aware that as the RP progresses, these individuals will become increasingly dependent on the auditory input. Those children with USH1 who have received early implantation generally display phonological and lexical skills developed to a higher extent than other children with CI of the same age, at some instances similar to those of children with NH. This could be an indication of that there are separate groups of CI-users, possibly with different needs in rehabilitation and education. Further research is necessary to explore the findings of this study and to examine the possibilities and limitations of the possibly different groups of CI-users. References [1] K. Mo¨ller, Impact on participation and service for persons with deaf-blindness, ¨ rebro Doctoral Thesis, Swedish Institute of Disability Research, Universities of O and Linko¨ping, 2008. [2] M. Sadeghi, Usher syndrome; prevalence and phenotype–genotype correlations, Doctoral Thesis, Department of Audiology/Institute of Selected Clinical Sciences, University of Gothenburg (Go¨teborg), 2005. [3] H. Kremer, E. van Wijk, T. Ma¨rker, U. Wolfrum, R. Roepman, Usher syndrome: molecular links of pathogenesis, protein and pathways, Hum. Mol. Genet. 15 (2) (2006). [4] R. Pennings, Hereditary deaf-blindness: clinical and genetic aspects, Doctoral Dissertation, University of Nijmegen, Netherlands, 2004. [5] C. Hederstierna, C. Mo¨ller, A. A˚hlman, R. Lundberg, U. von Do¨beln, The prevalence of Connexin 26 mutations in the Swedish population, J. Audiol. Med. 3 (2005) 154–158. [6] N.R. Peterson, D.B. Pisoni, R.T. Miyamoto, Cochlear implants and spoken language processing abilities: review and assessment of the literature, Restor. Neurol. Neurosci. 28 (2010) 237–250. [7] L. Asker-A`rnasson, T. Ibertsson, M. Wass, A˚. Wengelin, B. Sahle´n, Picture-elicited written narratives, process and product, in 18 children with cochlear implants, Commun. Disord. Quart. 31 (4) (2010) 195–212. [8] B. Lyxell, M. Wass, B. Sahle´n, T. Ibertsson, L. Asker-A´rnason, I. Uhle´n. Hearing and cognitive development in deaf and hearing-impaired children: effects of intervention, in: G. Celesia (Ed.), Handbook of Clinical Neurophysiology, vol. 10, 2012, in press. [9] J.G. Nicholas, A.E. Geers, Will they catch up? The role of age at implantation in the spoken language development of children with severe to profound hearing loss, J. Speech Lang. Hear. Res. 50 (2007) 1048–1062. [10] B. Schramm, A. Bohnert, A. Keilmann, Auditory, speech and language development in young children with cochlear implants compared with children with normal hearing, Int. J. Pediatr. Otorhinolaryngol. 74 (7) (2010) 812–819.
C. Henricson et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1449–1457 [11] L.j. Spencer, J.B. Tomblin, Evaluating phonological processing skills in children with prelingual deafness who use cochlear implants, J. Deaf Stud. Deaf Educ. 14 (1) (2009). [12] M. Wass, Children with cochlear implants, Doctoral Dissertation, Linkopings University (Swedish Institute of Disability Research), Linkoping, 2009. [13] T.P. Alloway, S.E. Gathercole, C. Willis, A.-M. Adams, A structural analysis of working memory and related cognitive skills in young children, J. Exp. Child Psychol. 87 (2004) 85–106. [14] A. Baddeley, Working memory: theories, models, and controversies, Annu. Rev. Psychol. 63 (2012) 1–29. [15] A. Baddeley, The episodic buffer: a new component of working memory? Trends Cogn. Sci. 4 (11) (2000). [16] A. Baddeley, Working memory and language: an overview, J. Commun. Disord. 36 (2003) 189–208. [17] M. Wass, T. Ibertsson, B. Lyxell, B. Sahle´n, M. Ha¨llgren, B. Larsby, et al., Cognitive and linguistic skills in Swedish children with cochlear implants measures of accuracy and latency as indicators of development, Scand. J. Psychol. 49 (2008) 559–576. [18] C. Johnson, U. Goswami, Phonological awareness, vocabulary, and reading in deaf children with cochlear implants, J. Speech Lang. Hear. Res. 53 (2010) 237–261. [19] S. Gathercole, Nonword repetition and word learning: the nature of the relationship, Appl. Psycholinguist. 27 (2006) 513–543. [20] C. Jaquemont, S.K. Scott, What is the relationship between phonological shortterm memory and speech processing? Trends Cogn. Sci. 10 (11) (2006). [21] J.N. Towse, G.J. Hitch, N. Horton, K. Harvey, Synergies between processing and memory in children’s reading span, Dev. Sci. 13 (5) (2010) 779–789. [22] T. Ibertsson, U. Willstedt-Svensson, K. Radeborg, B. Sahle´n, A methodological contribution to the assessment of nonword repetition – a comparison between children with specific language impairment and hearing impaired children with
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hearing aids or cochlear implants, Logoped. Phoniatr. Vocol. 33 (4) (2008) 168– 178. U. Willstedt-Svensson, A. Lo¨fqvist, B. Almqvist, B. Sahle´n, Is age at implant the only factor that counts? The influence of working memory in lexical and grammatical development in children with cochlear implants, Int. J. Audiol. 43 (2004). A. Sharma, A.A. Nash, M. Dorman, Cortical development, plasticity and re-organization in children with cochlear implants, J. Commun. Disord. 42 (2009) 272–279. A. Kral, A. Sharma, Developmental neuroplasticity after cochlear implantation, Trends Neurosci. 35 (2012) 111–122. T.P. Nikolopoulos, S.M. Archbold, G.M. O’Donoghue, Does cause of deafness influence outcome after implantation in children? Pediatrics 118 (2006) 1350– 1356. A. Adato, V. Michel, K. Yoshiaki, J. Reiners, K.N. Alagramam, D. Weil, et al., Interactions in the network of Usher syndrome type 1 proteins, Hum. Mol. Genet. 14 (2005) 347–356. B. Boe¨da, A. El-Amraoui, A. Bahloul, R. Goodyear, L. Daviet, S. Blanchard, et al., Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair bundle, EMBO J. 21 (24) (2002) 6689–6699. J. Reiners, E. van Wijk, T. Ma¨rker, U. Zimmermann, K. Ju¨rgens, H. te Brinke, et al., Scaffold protein harmonin (USH1C) provides molecular links between Usher syndrome type 1 and 2, Hum. Mol. Genet. 14 (24) (2005) 3933–3943. M. Schwander, B. Kachar, U. Mu¨ller, The cell biology of hearing, J. Cell Biol. 190 (1) (2010). A.D. Martı´nez, R. Acun˜a, V. Figueroa, J. Maripillan, B. Nicholson, Gap-junction channels dysfunction in deafness and hearing loss, Antioxid. Redox Signal. 11 (2) (2008). T. Ibertsson, K. Hansson, L. Asker-A`rnason, B. Sahle´n, Speech recognition, working memory and conversation in children with cochlear implants, Deaf Educ. 11 (3) (2009) 132–151.
Contents lists available at SciVerse ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Cognitive skills in children with Usher syndrome type 1 and cochlear implants Cecilia Henricson a,b,d,*, Malin Wass a,b,d, Bjo¨rn Lidestam b,d, Claes Mo¨ller a,b,c, Bjo¨rn Lyxell a,b,d a
Swedish Institute for Disability Research (SIDR), Sweden Linnaeus Centre for Research on Hearing and Deafness (HEAD), Sweden c Audiological Research Centre, O¨rebro University Hospital, O¨rebro University, Sweden d Department of Behavioral Sciences and Learning, Linko¨ping University, Linko¨ping, Sweden b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 22 March 2012 Received in revised form 30 May 2012 Accepted 3 June 2012 Available online 12 July 2012
Introduction: Usher syndrome is a genetic condition causing deaf-blindness and is one of the most common causes of syndromic deafness. Individuals with USH1 in Sweden born during the last 15 years have typically received cochlear implants (CI) as treatment for their congenital, profound hearing loss. Recent research in genetics indicates that the cause of deafness in individuals with Usher type 1 (USH1) could be beneficial for the outcome with cochlear implants (CI). This population has not previously been the focus of cognitive research. Objective: The present study aims to examine the phonological and lexical skills and working memory capacity (WMC) in children with USH1 and CI and to compare their performance with children with NH, children with hearing-impairment using hearing-aids and to children with non-USH1 deafness using CI. The participants were 7 children aged 7–16 years with USH1 and CI. Methods: The participants performed 10 sets of tasks measuring phonological and lexical skills and working memory capacity. Conclusions: The results indicate that children with USH1 and CI as a group in general have a similar level of performance on the cognitive tasks as children with hearing impairment and hearing aids. The group with USH1 and CI has a different performance profile on the tests of working memory, phonological skill and lexical skill than children with non-USH1 deafness using CI, on tasks of phonological working memory and phonological skill. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Children with cochlear implants Usher syndrome type 1 Spoken language Cognition Phonological skills Lexical skills Working memory
1. Introduction Usher syndrome (USH) is a genetic condition affecting hearing, balance and vision with a prevalence of 3.0–3.6/100,000 newborns in Sweden [1,2]. It is one of the most common causes of syndromic deafness [2,3], and there are three different clinical types (types 1–3) [1,2,4]. Usher type 1 (USH1) has a congenital, profound bilateral deafness, lack of bilateral vestibular function (areflexia) and retinitis pigmentosa (RP), causing degeneration of the rods of the retina, with impaired night vision, progressive narrowing of visual field and loss of peripheral vision as a result [2,4]. Most individuals with Usher syndrome have remaining central vision of 5–108 in late adulthood [2,4]. Type 2 displays a congenital, moderate to severe hearing loss which remains rather stable through life, RP, and normal vestibular function [2,4].
* Corresponding author at: Department of Behavioral Sciences and Learning, Linko¨pings Universitet, S-582 35 Linko¨ping, Sweden. Tel.: +46 13 28 20 91; fax: +46 13 28 21 45. E-mail address: [email protected] (C. Henricson). 0165-5876/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2012.06.020
Usher syndrome type 3 can display both pre- and post-lingual onsets of progressive moderate to severe hearing loss, as well as progressive loss of vestibular function and occasionally late onset of RP [2]. In the present study, focus is on children with USH1. The prevalence of congenital, syndromic and non-syndromic, deafness in Sweden is about 1–2/1000 newborns [5] and the vast majority of children (including children with USH1) are treated with cochlear implantation (CI), performed within the first two years of age. CI is an implantable biomedical device providing auditory sensation to individuals with profound sensori-neural hearing loss [6]. The outer parts consist of a microphone, a signal processor and (radio) transmitter. The implanted parts are a combined receiver and transmitter, placed beneath the skin in the bone of the back of the skull, as well as an array of electrodes that has been inserted into the coil of the inner ear. The cochlear implant converts the incoming sounds to electrical pulses which are transmitted through the electrodes [6]. There is an accumulating body of knowledge regarding the development of speech, language and cognitive skills in deaf and hearing-impaired children with CI [e.g. 7–9,6,10–12]. The findings indicate that the development of spoken language
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skills in the majority of children with CI is adequate to allow for verbal communication to be the primary mode of communication, and that these skills are likely to be more complex and better developed the earlier the implantation is done [8,9,6,10,11]. Previous research has not focused on development of speech, language and cognitive skills in the population of children with USH1 and our level of knowledge is thus limited with respect to their cognitive development. Exploring aspects of cognition related to hearing and language in this group has another caveat as well. Children who receive cochlear implants are typically regarded as one population in research and rehabilitation, and this study represents an attempt to explore whether this assumption is valid. In the present study, focus is on working memory (WM) and phonological and lexical skills. These cognitive abilities are important for the development of complex and composite skills such as communication and reading [13]. The concept of working memory refers to the simultaneous storage and processing of information [14]. Working memory is a theoretical construct implying a continuous on-line ability, used in almost all everyday situations [13–16]. It is a memory system that includes four components: a central executive, a visual loop, a phonological loop and an episodic buffer [14]. The central executive is responsible for planning, co-ordination and execution of activities within the working memory system. The phonological loop is responsible for manipulation, storage and processing of auditory information. The visual loop serves a similar purpose for visual or spatial information. The episodic buffer is a link between new, incoming information and old information stored in long-term memory. The phonological loop is a subsystem in WM that simultaneously stores and processes auditory input, for example speech sounds [i.e. 16]. Phonological WM is important in particular during vocabulary development [13,16] and Wass et al. [17] found that children with CI had significantly poorer phonological WM than children with normal hearing, corroborating other studies on spoken language skills in children with CI [e.g. 11,18]. However, it is important to note that in the study by Wass et al. [17] there was only a small significance for the difference between the groups on general WM, indicating that some children with CI reach the same level of development of general WM as children with NH, and there was no difference between the groups regarding visual WM. Phonological skills are important for language development [9,6,19,20]. Phonological skill is an umbrella term implying the processing and decision-making about phonological information [17]. The process of finding and retrieving verbal labels from long term memory (i.e. matching incoming speech stimuli to the correct word and its meaning) is termed lexical access, and this cognitive ability correlates with phonological skill and phonological WM [17]. Wass et al. [17] found that children with cochlear implants display significantly poorer phonological skills and lexical access than children with NH. Most of the phonological skills and lexical access are fully developed by age 5–6 in children with NH and typical language development [e.g. 16,17,19].
The aim of this study was to examine the level of development of phonological and lexical skills, and working memory capacity (WMC), in a population of children with Usher type I using CI. The performance of this group was compared to that of children with normal hearing (NH), to children with hearing-impairment using hearing-aids, and to children with non-USH1 deafness using CI.
2. Material and methods The participants were recruited from a register at the ¨ rebro, Audiological Research Centre, University Hospital of O Sweden and from the family organization for children with CI in Sweden, Barnplantorna. The study was approved by the regional ¨ rebro. Care-giver informed consent ethic committee of Uppsala-O in written form was received from all the participants. A letter of information directed to the children was also included in the information about the study given to the care-givers of the participants. 2.1. Participants Inclusion criteria for the group with USH1 were (1) a confirmed diagnosis of USH1, (2) age between 6 and 16 years, (3) no known (except for visual) co-existing disability, (4) performance within, or above, their age norm on block design from WISC-III, and (5) Swedish as the primary language and no known language impairment. The diagnosis of USH1 had been set clinically and genetically. Of the seven participants, 2 had USH1b, and 3 had USH1d. For two participants there was not yet a confirmed genetic diagnosis. No visual data on the participants were available for this study, but according to information from parents and participants, the visual problems were not yet large enough to interrupt performance at situations such as those experienced during testing. Regarding the control group with CI inclusion criteria were (1) a diagnosis or cause of profound deafness other than Usher syndrome, (2) age between 6 and 14 years (3) no known coexisting disability, (4) performance within, or above, their age norm on block design from WISC-III, and (5) Swedish as the primary language and no known language impairment. The 33 children in the control group with CI had diagnoses as follows: 20 had unspecified congenital deafness, 6 had unspecified congenital and progressive severe hearing loss, 3 had acquired deafness due to CMV-infection, 2 had LVAS, 1 had PN Meningitis, 1 had Wardenbu syndrome and 1 had Mondini malformation. The control group with hearing impairment using hearing aids had similar inclusion criteria as the control group with CI, though the first criteria was a confirmed hearing loss requiring hearing aid. For the control group with normal hearing the inclusion criteria were (1) no known existing hearing problems and no ear infections during the last three months, (2) age between 6 and 12 years, and (3) Swedish as the primary language and no known language impairment. The highest age for inclusion is lower for this group than the others,
Table 1 Demographics of the participants with Usher syndrome type 1. Participant
Age (y.:mo.)
Age at 1st CI
Age at 2nd CI
Language
Bilateral
1 2 3 4 5 6 7
7:6 8:0 8:1 8:10 12:4 12:11 15:11
20 months 18 months 12 months 9.5 months 39 months 32 months 4 years
22 months 30 months 30 months 18 months – 8.5 years 12 years
Spoken Sw. Spoken Sw. Spoken Sw. Spoken Sw. Sign supported Sw. Spoken Sw. SSL/spoken Sw.
Yes Yes Yes Yes No Yes Yes
Sw., Swedish; SSL, Swedish sign language.
C. Henricson et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1449–1457 Table 2 Description of the groups using CI.
Age at diagnosis (y.:mo.) n Mean SD Range Age at 1st CI (y.:mo.) n Mean SD Range Age at 2nd CI (y.:mo.) n Mean SD Range Age at testing (y.:mo.) n Mean SD Range
USH1
Control group CI
7 1:1 0:10 1:11
33 1:2 0:10 3:0
7 1:1 1:2 3:2
33 3:6 2:0 8:1
6 4:8 4:3 10:6
21 6:11 1:8 6:10
7 10:3 3:0 8:5
33 8:11 2:0 7:9
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language pathologists for percent consonants correctly reproduced (pcc). The scoring was done in the same way for the repeated items in Serial Recall of Non-words but the task in this test was for the participant to repeat back increasing series of one-syllable non-words. Complex span (i.e. simultaneous storing and processing of information) was measured by Sentence Completion and Recall [21]. The participants listened to series of 2–5 incomplete sentences and were asked to fill in the last word (e.g. ‘‘Tomatoes are red, crocodiles are. . .’’) and memorize it for later recall, the result of the test being number of correctly recalled words. Visuo-spatial working memory was measured by the Visual Matrix Pattern test [17], in which a 5 5 matrix of grey colored cells is displayed. A set number of cells switch simultaneously to black color, starting at 1 and increasing every third trial up to a maximum of 8 cells, and disappear after short display. The participant is then asked to click the cells which were previously black. The score is the highest number of cells successfully identified by the participant at two of the three trials. 2.4. Phonological skills
since piloting of the tests showed ceiling effects for children with normal hearing above age 12. The groups consist of (1) 7 children with USH1, (2) 33 children with non-USH1 deafness using CI, (3) 43 children with hearing impairment (HI) using hearing aids (HA) and (4) 120 children with NH. For group 3, the mean age at testing was 9 years and 3 months (SD = 1 y. 9 mo.) and for group 4 mean age at testing was 9 years and 2 months (SD = 1 y. 8 mo.). The demographics of the children with USH1 and CI are displayed in Table 1. See Table 2 for information about the two groups with CI regarding ages at diagnosis, implantation and testing. 2.2. Methods The participants were tested at the Audiological Research ¨ rebro, in their school setting, or in their home. The test Centre in O block-design from WISC-III was used to ascertain that the cognitive performance of the participating children was within the norm with respect to their age group. The tests were administered on a lap-top computer and consisted of a test battery designed to measure phonological skills, lexical skills, phonological WM, complex WM and visuospatial WM, called the Sound Information Processing Systems (SIPS) [17]. All of the tests in SIPS, except for a measure of visual WM and one of passive naming, were presented in auditory-only in the same female speaker voice. The auditory stimuli were presented with loudspeakers (Logitech S-100) which were set by the child to a level of comfortable loudness [cf. 8,17]. Short descriptions of each category of tests are given here. An extensive description of the tests and procedures is given in Wass et al. [17].
Phonological skills were measured by three tests, each designed to measure different aspects of phonological skills. The tests used were: Non-word Discrimination, Phonological Representations, and Phoneme Identification [17]. The task in Non-word Discrimination was for the participant to press a button if the presented pair out of 16 non-words were identical. In order to achieve maximum score (8) on the test, the participant had to discriminate correctly for all pairs, same and different (i.e. push when identical and not push button when pairs were different). Real words were used in the test Phonological Representations in which the participant is asked to report on when a familiar word is pronounced correctly out of several options. To make certain that the participant was familiar with the word s/he was shown an illustration of the word (i.e. ‘‘sofa’’) and asked to say what was depicted. The task in Phoneme Identification was to press a button if there was a specific language sound within the auditorily presented non-words (i.e. ‘‘is there ‘r’ in ‘federur’?’’ or ‘‘is there ‘s’ in ‘ho¨ntpule’?’’). 2.5. Lexical access This ability was measured by three tests: Word-spotting, Semantic Decision Making and Word Mobilization. In word-spotting the participant was asked to push a button as soon as s/he identified a real word among series of one syllable non-words. Semantic Decision Making required the participant to push a button when there was a word adhering to a specific, defined category (i.e. ‘‘push the button when you hear something that is an animal’’) and hence uses real words as stimuli. Word Mobilization also used real words and the task was to identify the matching picture among four alternatives after a word had been presented. 2.6. Statistics
2.3. Working memory The tasks designed to measure WM were all presented in auditory only, except for Visual Matrix Pattern test. Phonological WM was measured by Non-word Repetition and by Serial Recall of one-syllable non-words. In order to ensure that the results were not affected by vocabulary or word knowledge (or both combined), non-words were used as stimuli in these two sets of tasks tapping phonological WM. In the test Non-word Repetition, the participant is asked to repeat back non-words of increasing syllable length. The repetition attempts were recorded at the test-occasion and scored off-line by speech and
The results from the present study were computed in two different ways. First, the confidence intervals of the groups on a 0.05 significance level (CI95) were calculated and compared in order to establish possible group differences for mean performance. Secondly, the pattern of performance among the individuals with USH1 is described in relation to linear models of the mean values of the control groups (i.e. regression lines). The performance in the different tasks is in these analyses described as a function of age, as the variation of performance across age is different in the group with USH1 and for control groups. The performance of the children with USH1 is presented in Figs. 1–3.
[(Fig._1)TD$IG]
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Fig. 1. Results on measures of working memory in relation to age in months. The individuals’ values in the three control groups are displayed. Linear regression models of the control groups’ means are displayed, with confidence intervals (CI95) of the model. The individual performances of the participants with Usher syndrome type 1 are shown in each panel, each participant with a unique number (1–7).
[(Fig._2)TD$IG]
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Fig. 2. Results on measures of lexical skill in relation to age in months. The individuals’ values in the three control groups are displayed. Linear regression models of the control groups’ means are displayed, with confidence intervals (CI95) of the model. The individual performances of the participants with Usher syndrome type 1 are shown in each panel, each participant with a unique number (1–7).
3.1. Comparisons of group means
group with CI. No significant differences were obtained between the USH1 group and the groups of children with HI, and children with NH on this task. For the two phonological working-memory tasks, the children with NH scored significantly higher than all the other three groups. No significant difference in performance emerged between the children with USH1, the control group with CI, and the children with hearing-impairment, on the tasks measuring phonological WM. For the visual working memory task, performance was similar between the USH1 group and the three other groups.
3.1.1. Working memory capacity The children with USH1 scored significantly higher on general WM (Sentence Completion and Recall), than the control
3.1.2. Lexical skills The children with USH1 scored significantly higher than the control group with CI on one of three lexical tasks
3. Results The results will be presented in two parts. First, the means for the groups, and the statistically significant differences of the means between the group with USH1 and the control groups will be presented (see Table 3). This is followed by an account of the performance of the individuals with USH1 in relation to the control groups (see Figs. 1–3).
[(Fig._3)TD$IG]
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Fig. 3. Results on measures of phonological skill in relation to age in months. The individuals’ values in the three control groups are displayed. Linear regression models of the control groups’ means are displayed, with confidence intervals (CI95) of the model. The individual performances of the participants with Usher syndrome type 1 are shown in each panel, each participant with a unique number (1–7).
(Word Mobilization). No other differences between the group with USH1 and the three control groups proved to be significant on these tasks. 3.1.3. Phonological skills The children with USH1 scored significantly higher than the control group with CI on the Non-Word Discrimination task, while no significant difference was found between the children with USH1 and the children with NH or HI. No significant difference was found in the Phoneme Identification task or the task Phonological Representations between the USH1 group and the other groups. However, it should be noted that the both
groups of deaf children with CI scored significantly lower on these tasks compared to the NH group. 3.2. Performance of the individuals with USH1 in relation to control groups and age The performance of the participants with USH1 is presented as number of individuals in the group performing above, on or below the 95% confidence bands of the control group’s regression lines. Results are displayed in Figs. 1–3. Each panel of a figure displays the performance of the individuals from a specific control group, as well as the regression line with CI95 for that group. The
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Table 3 Mean values and confidence intervals of the groups, and number of participants in each group on every measure. Working memory
USH1 NH HI using HA Deaf CI
Visual Matrix Pattern
Sentence Completion and Recall
Serial Recall of Non-words (pcc)
Non-word Repetition (pcc)
n
M (CI95)
n
M (CI95)
n
M (CI95)
n
M (CI95)
7 120 43 33
5.0 4.7 4.4 3.9
7 120 43 28
12.7 (10.7–14.7) 12.3 (11.9–12.8) 12.0 (11.3–12.8) 8.4 (6.9–10.0)
7 116 43 26
33.6 57.9 45.7 28.2
7 117 43 26
58.1 88.2 76.5 39.0
(3.3–6.6) (4.4–4.9) (4.0–4.8) (3.4–4.5)
(16.5–50.7) (55.8–60.1) (41.7–49.7) (25.2–33.3)
(41.6–74.6) (86.9–89.5) (73.1–80.0) (32.0–45.8)
Lexical skills Word Mobilization
USH1 NH HI using HA Deaf CI
Word-spotting
Semantic Decision Making
n
M (CI95)
n
M (CI95)
n
M (CI95)
6 120 43 38
7.8 8.7 8.5 5.9
4 120 43 31
4.8 7.9 6.3 3.7
7 120 43 36
22.9 28.3 28.3 24.8
(6.6–9.1) (8.6–8.8) (8.3–8.8) (5.1–6.6)
(1.0–8.5) (7.7–8.1) (5.7–6.9) (2.96–4.5)
(17.5–28.2) (28.1–28.5) (28.0–28.6) (23.5–26.1)
Phonological skills
USH1 NH HI using HA Deaf CI
Phonological Representations
Non-word Discrimination
Phoneme Identification
n
M (CI95)
n
M (CI95)
n
M (CI95)
5 46 43 15
15.8 17.9 17.3 15.5
6 120 43 28
7.2 7.9 7.1 4.8
5 46 43 13
8.8 (5.1–12.5) 11.4 (11.2–11.7) 11.7 (8.6–14.8) 7 (4.9–9.1)
(11.9–19.7) (17.9–18.0) (17.1–17.5) (14.2–16.9)
(6.1–8.2) (7.8–7.9) (6.7–7.5) (3.9–5.6)
performance of each child with USH1 and CI is superimposed on the performance of the control groups.
and to the control group with CI on another set of tasks (see Fig. 3, phonological skill).
3.2.1. Working memory The majority of the participants with USH1 perform similar to children with HI using HA, and children with NH of the same age, on the tasks measuring general WM (Fig. 1, general WM). Regarding visual WM the range of performance among the children with USH1 is wider, with the performance of one participant exceeding, and two participants performing below, the three control groups (Fig. 1, visual WM). The results from the two sets of tasks measuring phonological WM showed that the children with USH1 in general had higher performance than the control group with CI on Non-word Repetition, while the two groups with CI had similar performance on Serial Recall of Nonwords (Fig. 1, phonological WM). Only two of the participants with USH1 had performance above, and similar to, that of children with NH or HI using HA, while the other five performed below these groups (Fig. 1, phonological WM).
4. Discussion
3.2.2. Lexical skill The results showed a high degree of variation in performance among and within the participants with USH1 on the tasks measuring lexical skill. One participant had performance similar to that of children with NH and children with HI using HA, on two out of three sets of tasks. Several of the participants displayed higher performance than the control group with CI on two of the tasks measuring lexical skill (see Fig. 2, lexical skill, Word Mobilization and Semantic Decision Making). 3.2.3. Phonological skill The results display that two individuals with USH1 had consistently higher scores than the control group with CI, and a performance similar to that of the control group with HI using HA (see Fig. 3, phonological skill). The other participants with USH1 varied in performance on the different sets of tasks, performing similar to the control groups with NH or HI using HA on some tasks
The present study examined working memory capacity, phonological and lexical skills in children with USH1 and CI. The performance of 7 children with USH1 and CI was related to populations of children with normal hearing, to children with hearing impairment using hearing aids and to children with nonUSH1 deafness using CI. In sum, the general pattern of results showed that, as a group, the children with USH1 have performance levels on the cognitive tests used in the study that do not differ significantly from the control group of children with NH, except for specific abilities such as phonological working memory. The control group with NH had, as expected, significantly higher results on phonological working memory than the three other groups (see [7,17] for similar results). Though there is a high variation in performance among the children with USH1, they receive higher scores on specific aspects of phonological WM and phonological skill than the control group of children with CI. Working memory capacity, lexical and phonological skills are abilities that develop and refine during childhood [13,21], thus, it was important to examine developmental trends in the control groups in order to see how the individuals with USH1 and CI performs with respect to their chronological age. Most of the participants with USH1 displayed a performance level on general, and visual, working memory tasks that is similar to that of children with NH and to children with HI using HA of the same age. However, the results of the children with USH1 could seem contradictory, since they outperform the group of children with non-syndromic deafness and CI on one measure but perform similar, poor results on the other. The two tasks of phonological working memory differ such that in the Non-word Repetition tasks the non-words have a complex syllable structure and contain supra-segmental properties (i.e. stress patterns and intonations [17,20,22]) whereas
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in Serial Recall of Non-words the non-words are of simple CVCstructure [17,20,22]. In Serial Recall of Non-words the majority of individuals with USH1 perform similarly to the control group with CI, while six out of the seven children with USH1 perform higher scores on Non-word Repetition. This may indicate that the children with USH1 are able to make more use of the suprasegmental properties than the deaf children with CI. The results also display that the children with USH1 who have had early implantation (participants 1–4; age at implantation < 2 years) tended to perform in line with the expected performance level for children with HI using HA, or even in some cases as children with NH, of the same age. This level of performance is in contrast to the children with USH1 who received implants at later ages (participants 5–7). The children with later implantation tended to perform similar to other deaf children with CI of the same age on tasks assessing phonological working memory and phonological skill. These findings corroborate previous research [17,23] that noted a lag in the development of phonological and lexical skills, particularly for children with late implantation (age > 3). Similarly, Sharma et al. [24], using an ERP-paradigm, found that the brain responses to speech sounds were deviant in children with this late implantation in comparison to children with early implantation, whose brain response was similar to that of children with NH (see also Kral and Sharma [25]). Similar to previous research [6,7,9], this may indicate an atypical development of phonological working memory and phonological skills in children with late implantation. An atypical development of these abilities and skills could influence the development of composite skills such as reading [17]. Lack of auditory stimulation, as well as a less detailed signal from the cochlear implant, is generally suggested as parts of the explanation to the deviant development of spoken language skills in individuals with CI [e.g. 6,12,23,26]. However, one main finding of the present study is that the participants with USH1 have better developed phonological and lexical skill, and that one aspect of phonological working memory appears to be more capacious in the children with USH1 than in the control group of CI-users. The performance of the group with USH1 was actually more similar to that of children with HI using HA than to other deaf children with CI across most tasks. These findings could be indications of individuals with USH1 having different prerequisites for hearing with CI, than individuals with other types of deafness. Recent research on animal models with Usher syndrome has revealed the phenotypic expression and functional consequences of the mutated genes causing USH1 [e.g. 27–30]. The results indicate a disruption in the function of the stereocilia of the IHC in the cochlea, causing the profound hearing loss [30]. In for example GJB2 (Connexin 26), a nonsyndromic cause of deafness, the mutations seem to primarily affect the cell bodies of the IHC, and aspects of the membranes separating the Scala media from the Scala tympani [31]. If there are remaining IHC in humans with USH1, these could be important in the functioning with a cochlear implant (CI). It is thought that a CI in typical cases stimulates the spiral ganglion cells. There is a possibility that the CI not only stimulates the spiral ganglion cells, but also that the IHCs interact with the electrical stimulation, i.e. by flexing and firing neural pulses, thus, allowing for more nuanced auditory stimulation than other deaf individuals using CI have. A more detailed auditory signal would, in turn, be beneficial for the development of cognitive skills associated with hearing [17,32]. Following this, the higher performance of the group with USH1 on tasks of phonological working memory and phonological and lexical skills compared to the control group of CI-users could be explained. The children with USH1 participating in this study are also likely to benefit from the fact that they have received an early
diagnosis, which means that there are early interventions and awareness of that these individuals will lose vision and thus will become increasingly dependent on their CIs. This awareness could trigger great efforts to build the children’s competence in using their implants, which in addition to a potentially more detailed auditory signal would benefit these children’s development of the cognitive abilities associated with hearing. The idea of existing but non-operational inner hair cells in humans with USH1 is intriguing, and hopefully future research projects will explore the findings of the present study and what reasons there could be to the group differences. More profound knowledge regarding the morphology and the physiology of OHC and IHC in Usher syndrome is also needed. Given the small sample of participants with USH1 in this study, more research is needed in order to validate and replicate the findings. However, the seven participants comprise a fairly large proportion of the Swedish population with USH1 in the age of 6–16 years, and thus the findings are interesting despite the limitation of the small sample size. Also, the data has been analyzed on two levels, group and individual, and both analyses converge to the same pattern; the participants with USH1 perform better on specific tasks than their peers with CI. This could be claimed to further validate the findings. In conclusion, the findings of the present study indicate that some aspects of phonological WM and phonological skill are better developed in the participants with USH1. This could be an indication of prerequisites for developing more defined phonological skills than other deaf children with CI. It could also be the result of more focused interventions due to the fact that the children and their environment in an early stage are aware that as the RP progresses, these individuals will become increasingly dependent on the auditory input. Those children with USH1 who have received early implantation generally display phonological and lexical skills developed to a higher extent than other children with CI of the same age, at some instances similar to those of children with NH. This could be an indication of that there are separate groups of CI-users, possibly with different needs in rehabilitation and education. Further research is necessary to explore the findings of this study and to examine the possibilities and limitations of the possibly different groups of CI-users. References [1] K. Mo¨ller, Impact on participation and service for persons with deaf-blindness, ¨ rebro Doctoral Thesis, Swedish Institute of Disability Research, Universities of O and Linko¨ping, 2008. [2] M. Sadeghi, Usher syndrome; prevalence and phenotype–genotype correlations, Doctoral Thesis, Department of Audiology/Institute of Selected Clinical Sciences, University of Gothenburg (Go¨teborg), 2005. [3] H. Kremer, E. van Wijk, T. Ma¨rker, U. Wolfrum, R. Roepman, Usher syndrome: molecular links of pathogenesis, protein and pathways, Hum. Mol. Genet. 15 (2) (2006). [4] R. Pennings, Hereditary deaf-blindness: clinical and genetic aspects, Doctoral Dissertation, University of Nijmegen, Netherlands, 2004. [5] C. Hederstierna, C. Mo¨ller, A. A˚hlman, R. Lundberg, U. von Do¨beln, The prevalence of Connexin 26 mutations in the Swedish population, J. Audiol. Med. 3 (2005) 154–158. [6] N.R. Peterson, D.B. Pisoni, R.T. Miyamoto, Cochlear implants and spoken language processing abilities: review and assessment of the literature, Restor. Neurol. Neurosci. 28 (2010) 237–250. [7] L. Asker-A`rnasson, T. Ibertsson, M. Wass, A˚. Wengelin, B. Sahle´n, Picture-elicited written narratives, process and product, in 18 children with cochlear implants, Commun. Disord. Quart. 31 (4) (2010) 195–212. [8] B. Lyxell, M. Wass, B. Sahle´n, T. Ibertsson, L. Asker-A´rnason, I. Uhle´n. Hearing and cognitive development in deaf and hearing-impaired children: effects of intervention, in: G. Celesia (Ed.), Handbook of Clinical Neurophysiology, vol. 10, 2012, in press. [9] J.G. Nicholas, A.E. Geers, Will they catch up? The role of age at implantation in the spoken language development of children with severe to profound hearing loss, J. Speech Lang. Hear. Res. 50 (2007) 1048–1062. [10] B. Schramm, A. Bohnert, A. Keilmann, Auditory, speech and language development in young children with cochlear implants compared with children with normal hearing, Int. J. Pediatr. Otorhinolaryngol. 74 (7) (2010) 812–819.
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