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Relation between language, audio–vocal psycholinguistic abilities and P300 in children having specific language impairment
International Journal of Pediatric Otorhinolaryngology 75 (2011) 1117–1122
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Relation between language, audio–vocal psycholinguistic abilities and P300 in children having specific language impairment Elham Ahmed Shaheen a,*, Sahar Saad Shohdy a, Mahmoud Abd Al Raouf b, Shereen Mohamed El Abd c, Asmss Abd Elhamid a a b c
ENT Department, Phoniatric Unit, Faculty of Medicine, Cairo University, Egypt ENT Department, Faculty of Medicine, Cairo University, Egypt ENT Department, Audiology Unit, Faculty of Medicine, Cairo University, Egypt
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 April 2011 Received in revised form 1 June 2011 Accepted 2 June 2011 Available online 30 June 2011
Specific language impairment is a relatively common developmental condition in which a child fails to develop language at the typical rate despite normal general intellectual abilities, adequate exposure to language, and in the absence of hearing impairments, or neurological or psychiatric disorders. There is much controversy about the extent to which the auditory processing deficits are important in the genesis specific language impairment. The objective of this paper is to assess the higher cortical functions in children with specific language impairment, through assessing neurophysiological changes in order to correlate the results with the clinical picture of the patients to choose the proper rehabilitation training program. Subjects and method: This study was carried out on 40 children diagnosed to have specific language impairment and 20 normal children as a control group. All children were subjected to the assessment protocol applied in Kasr El-Aini hospital. They were also subjected to a language test (receptive, expressive and total language items), the audio–vocal items of Illinois test of psycholinguistic (auditory reception, auditory association, verbal expression, grammatical closure, auditory sequential memory and sound blending) as well as audiological assessment that included peripheral audiological and P300amplitude and latency assessment. The results revealed a highly significant difference in P300 amplitude and latency between specific language impairment group and control group. There is also strong correlations between P300 latency and the grammatical closure, auditory sequential memory and sound blending, while significant correlation between the P300 amplitude and auditory association and verbal expression. Conclusion: Children with specific language impairment, in spite of the normal peripheral hearing, have evidence of cognitive and central auditory processing defects as evidenced by P300 auditory event related potential in the form of prolonged latency which indicate a slow rate of processing and defective memory as evidenced by small amplitude. These findings affect cognitive and language development in specific language impairment children and should be considered during planning the intervention program. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Neurophysiology Illinois test P300 latency P300 amplitude Specific language impairment (SLI)
1. Introduction Language is a recent evolutionary phenomenon. In most children, the potential for language is present at birth [1]. Most children acquire language through environmental exposure to language without any special assistance. However, for some children with otherwise normal development, the acquisition of language proves
* Corresponding author at: ENT Department, Phoniatric Unit, Faculty of Medicine, Cairo University, 30 Milsa Towers, City Stars, Madinat Nasr, Cairo, Egypt. Tel.: +20 106423828; fax: +20 225319113. E-mail addresses: [email protected] (E.A. Shaheen), [email protected] (M. Abd Al Raouf), [email protected] (S. Mohamed El Abd), [email protected] (A. Abd Elhamid). 0165-5876/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2011.06.001
disproportionally difficult. Despite relatively normal nonlinguistic cognitive function and normal hearing, their language development is impaired. These children are considered to have specific language impairment (SLI) [2]. The failure of some children to master language at the normal rate has puzzled researchers for several decades. It was proposed that SLI is caused by low level auditory perceptual problems [3]. The criteria of diagnosis of specific language impairment that have been widely adopted either in part or in whole include a performance IQ (standard score) of at least 85 and at least one of the following: (a) a receptive language age (LA) score of at least 6 months below the mental age (MA) or chronological age (CA), whichever is lower; (b) a combined LA score of at least 12 months below the lower of MA or CA; or (c) an expressive LA score that is at least 12 months below the lower of MA or CA [4].
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Auditory information is translated by the sensory organs into neural activity, which in turn are processed and organized in the brain in different cortical and sub-cortical areas. In the thalamus, the information is processed and forwarded to the key cortical areas where more processing and integrating will take place [5]. The Auditory Brainstem Responses (ABR), measure the electrophysiologic activity from the 8th cranial nerve to the medial geniculate body of the brainstem [6]. Presentation of an auditory stimulus, such as a tone, triggers a sequence of neuronal events proceeding from the brainstem to cortex, reflection detection, classification, and interpretation of the sound. Late event related potentials (ERPs) can be used to index stage of auditory processing. P300 is the most used auditory event-related potential. This potential appears around 300 ms and requires attention, auditory discrimination and memory for its generation [7]. P300 has been considered an endogenous event related potential [8]. Endogenous responses depends both on the context within which the auditory stimuli are presented and attention of the subject [3]. It has been frequently claimed that children with specific language impairment have impaired central auditory processing, but there is much controversy about the role of such deficits in causing their language problems and it has been difficult to establish solid, replicable findings in this area. Insufficient attention has been paid to maturation aspects of auditory processing). The objective of this work is to assess the higher auditory cortical functions in children with specific language impairment, through assessing neurophysiological changes in order to correlate the results with the clinical picture of the patients to choose the proper rehabilitation training program. 2. Subjects and methods 60 pre-school Egyptian children were included in the study. Their ages ranged from 4 to 6 years, from the same socio-economic stratum. 40 children diagnosed as specific language impairment and 20 normal children to serve as a control group. The 2 groups were matched in age, gender and socioeconomic distribution. Consent was taken from the parents of all children participating in the study. Patient group consisted of 31 boys and 9 girls. Control group consisted of 16 boys and 4 girls. Testing the boys to girls difference was insignificant (chi 2 test = 0.95, P value > 0.05). Patient subjects meet the following criteria of specific language impairment [4]: 1 Normal peripheral hearing, 2 No neurological or psychological disorder, 3 No mental retardation, their intelligent quotient (IQ) is 90 or over (average), 4 Total language age is at least 12 months less than chronological age, and expressive language is at least 12 months less than the chronological age or the receptive language is at least 6 months less than the chronological age, control group criteria included: no history of delayed language development. Receptive, expressive and total language age matched their chronological age, normal development, and average IQ. All the participants were subjected to the language assessment protocol in the Phoniatric Unit, and to some neuro-physiological investigations applied in Audiology Unit, Kasr El Aini hospital in the period from 2006 to 2009, which included:
Examination: included: general, neurological, ear, nose and throat examination and preliminary language assessment. II Clinical diagnostic aids: 1 Arabic language test: This measures receptive age, expressive age, semantic age, pragmatic age and total language age [9] only receptive, expressive and total language age are included in this study. 2 Psychometric evaluation to measure the cognitive abilities: a Stanford Binet test 4th ed. [10] IQ = (mental age/chronological age) 100. b Illinois test of psycholinguistic abilities (ITPA) arabic edition [11] (2–10 years). In this study, only the audio–vocal items are studied which include: auditory reception, auditory association, verbal expression, grammatical closure, auditory sequential memory, auditory closure and sounds blending. The audio–vocal items can be arranged according to the structural complexity of items of the test as follows [12,13]: A Simple items: (knowledge dependent) auditory reception, verbal expression, grammatical closure, auditory association and auditory closure. B Complex items: (processing dependent) auditory sequential memory and sound blending. The test gives a psycholinguistic age and a diagnostic profile of psycholinguistic abilities. It also correlates highly with the childs intellectual abilities. It useful to assist in directing the remedial effort since it provides a profile or the abilities outlining the child particular strength and weaknesses. 3 Audiological assessment: i Pure tone audiometry, speech audiometry, immittancemetry, auditory brainstem response (ABR) [6] to confirm the normal peripheral hearing ability. ii Assessment of higher cognitive brain function using the event related potentials (ERP’s) namely auditory P300 amplitude and latency. Event related potential (P300): P300 was obtained with head phone TDH 39. An odd ball paradigm was used where the subject was instructed to react to occurrences of a tone (target) presented 20% of trials and to ignore a frequent tone present on other trials. P300 responses were obtained in response to the target stimuli. P300 amplitude: is the difference in microvolt between the point of maximum amplitude of the designated peak and stimulus baseline. P300 latency was measured from the time of stimulus onset to point of maximum amplitude of the chosen peak. Data were statistically described in terms of means standard deviation (SD), frequencies (number of cases) and percentages when appropriate. Comparison of quantitative variables between the study groups was done using Student t test for independent samples. For comparing categorical data, Chi square (x2) test was performed. Exact test was used instead when the expected frequency is less than 5 (Mont Carlo Exact method). Correlation between various variables was accomplished using Pearson moment correlation equation for linear relation. A probability value (P value) less than 0.05 was considered statistically significant. All statistical calculations were done using computer programs Microsoft Excel 2007 (Microsoft Corporation, NY, USA) and SPSS (Statistical Package for the Social Science; SPSS Inc., Chicago, IL, USA) version 15 for Microsoft Windows. 3. Results
I Elementary diagnostic procedures: Patient’s interview and history taking: including: personal, pre-natal, natal and post natal, developmental history, history of childhood illness and social behavior of the child.
Comparison of mean of chronological age between control group and children with SLI. The difference was insignificant. Chronological age of the control group ranged between of 4.40
E.A. Shaheen et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 1117–1122 Table 1 Comparison of the studied language items between the SLI cases and control group (Mont Carlo exact test). Item
SLI cases No.
Receptive language age 2–2.5 y 3 2.5–3 y 3–3.5 y 15 3.5–4 y 9 4–4.5 y 10 4.5–5 y 3 5–5.5 y 0 5.5–6 y 0 Expressive language age 2.5–3 y 6 3–3.5 y 15 3.5–4 y 16 4–4.5 y 1 4.5–5 y 2 5–5.5 y 0 Total language age 2 2.5–3 y 3–3.5 y 17 3.5–4 y 13 4–4.5 y 5 4.5–5 y 3 5–5.5 y 0
Control %
No.
%
7.5 37.5 22.5 25 7.5 0 0
0 0 0 6 3 9 2
0 0 0 30 15 45 10
15 37.5 40 2.5 5 0
0 0 0 5 11 4
0 0 0 25 55 20
5 42.5 32.5 12.5 7.5 0
0 0 0 6 8 6
0 0 0 30 40 30
Mont Carlo exact symbol significance
Table 2 Comparison between cases and controls regarding Illinois’ test of psycholinguistic abilities (audio–vocal items), P300 items and speech discrimination items under study. SLI cases (n = 40) Psycholinguistic items Auditory reception Auditory association Verbal expression grammatical closure Auditory sequential memory Auditory closure Sound blending Auditory items P300 amplitude P300 latency Speech discrimination
<0.001
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Controls (n = 20)
P value
3.45 0.52 3.23 0.41 3.36 0.50 3.08 0.51 2.68 0.41 3.23 0.44 3.45 0.41
4.86 0.55 4.71 0.53 4.92 0.61 4.92 0.63 4.77 0.70 4.79 0.73 4.65 0.85
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
8.65 1.79 365 29 81.78 3.39
12.73 1.12 278.4 27.9 91.70 2.43
<0.001 <0.001 <0.001
Data are represented as mean SD. Highly significant: P value < 0.001. SLI: specific language impairment. <0.001
<0.001
SLI: specific language impairment. %: is the percent within the group. Results revealed that there is a highly significant difference between the cases and the control group. The SLI group scored significantly lower than the control group in the receptive, expressive and total language age.
years and 5.80 years with a mean of 5.12 0.518 SD. Chronological age of the SLI group ranged between 4.11 years and 6.00 years with a mean of 5.24 0.618 SD, P value: 0.467 (P > 0.05). The results in (Table 1) revealed that there is a highly significant difference between the specific language impairment group and the control groups in the studied language items which included (receptive, expressive and total language age). The SLI group scored much lower than the control group. Table 2 revealed that the statistical comparison of the audio– vocal psycholinguistic items between the specific language impairment (SLI) and the control groups revealed highly significant differences in all items which included (auditory reception, auditory association, verbal excerption, manual excerptions auditory closure and auditory sequential memory). The SLI group scored much lower than the control group on comparing P300 amplitude and P300 latency is prolonged in SLI than in the control group. Speech discrimination item, the difference in all items is highly significant. Table 3 shows results of correlation within the SLI cases group revealed that there is a highly significant correlations between P300 amplitude with chronological, correlation of P300 amplitude
and latency with expressive language age are significant, correlations between P300 latency and amplitude with other items are insignificant. Within the control group, correlations between P300 amplitude as well as latency with chronological age as well as with language items under study are insignificant. Table 4 shows that within the SLI cases group, there is a significant correlation of P300 amplitude with auditory sequential memory while P300 latency has significant correlations with auditory closure and speech discrimination and a highly significant correlation with auditory sequential memory. Both P300 amplitude and latency have highly significant correlation with grammatical closure and sound blending. Otherwise correlations are insignificant. The correlations between the same items within the control group are insignificant. 4. Discussion In this study, P300 prolonged latency and small amplitude in the SLI group compared to the control group indicate the presence of higher cortical neurophysiological changes and late auditory perceptual processing stage deficit in these children. This means that there is slow processing of information and working memory defects that affected both language and cognition development. This can explain the low scores of the SLI children in both Language items and audio–vocal psycholinguistic items. This should be strongly considered in the construction of the rehabilitation program for SLI children. The significant difference in the receptive, expressive and total language age items between SLI children and control groups (Table 1) is explained by the poor general or the localized resource capacity theory of SLI children by [12]. These findings agreed with researchers
Table 3 Correlation between P300 amplitude and latency with chronological age and language items within each of SLI group and control group. Items
P300 amplitude Within group Correlation coefficient P value P300 latency Within group Correlation coefficient P value *
Chronological age
Receptive language age
Expressive language age
Total language age
SLI (40)
SLI (40)
SLI (40)
SLI (40)
0.601 0.001y
0.316 0.175
Control (20)
Control (20)
Control (20)
0.182 0.442
0.211 0.192
0.261 0.266
0.337 0.033*
0.398 0.082
0.274 0.088
0.248 0.292
0.212 0.370
0.296 0.206
0.096 0.68
0.510 0.021*
0.011 0.965
0.337 0.146
0.318 0.172
Means significant correlation (‘‘P’’ value < 0.05). Means highly significant correlation (‘‘P’’ value < 0.01). SLI: specific language impairment. y
Control (20)
0.095 0.690 0.489 0.029* 0.073 0.759 0.567 0.009y 0.122 0.608 0.504 0.023* 0.123 0.605 0.561 0.010y 0.153 0.519 0.574 0.008y 0.146 0.538 0.383 0.095 y
*
Means significant correlation (‘‘P’’ value < 0.05). Means highly significant correlation (‘‘P’’ value < 0.01). SLI: specific language impairment.
0.114 0.632 0.214 0.364 0.258 0.272
0.359 0.120
0.092 0.699 0.230 0.699 0.145 0.541 0.412 0.008y 0.289 0.217 0.267 0.096 0.203 0.390 0.339 0.033* 0.275 0.240 0.467 0.002z 0.316 0.175 0.438 0.005y 0.054 0.820 0.114 0.485 0.271 0.375
SLI Control SLI Control SLI Control SLI Control SLI Control SLI Control SLI Control SLI
0.271 0.091
P300 amplitude Within group Correlation coefficient P value P300 latency Within group Correlation coefficient P value
Sound blending Auditory closure Auditory sequential memory Grammatical closure Verbal expression Auditory association Auditory reception Items
Table 4 Correlation between P300 amplitude and latency and Illinois test of psycholinguistic abilities (audio–vocal items) and speech discrimination within each of SLI group and control group.
Control
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Speech discrimination
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who found that these children have fewer numbers of words to use spontaneously in expressing their ideas; they produce and comprehend fewer words than their normally developed peers [14]. The low auditory reception and auditory association ages in SLI children compared to the control group (Table 2) support the hypothesis of limitation of general resource receptive capacity in SLI children [15]. SLI children are slower in fast mapping and speed of processing of stimulus and need repeated exposure to the stimulus in to gain the meaning of the stimulus which leads to slow intake of language data from the input [16]. In this study, impaired auditory sequential memory in SLI children (Table 2) is in agreement with authors who used the complex memory span tasks [17]. Children with SLI showed marked deficits when the processing and storage demands of such tasks are verbal in nature [18], in non-word repetition task [19], and serial recall of digits and words [20]. The highly significantly low verbal expression and grammatical closure ages (Table 2) in the SLI compared to their control peers agreed with researchers who added that those SLI children may lack the basic vocal skills, and have inadequate vocabulary [21]. Our results are also in agreement with Pinke [22] who argued that domain-specific grammatical abilities develop from (genetic basis) pre-determined specialized mechanisms or neural circuitry provides evidence for the existence of a specialized grammatical subsystem in the brain, necessary for normal language development). In this study the low auditory closure and sound blending ages in the SLI group compared to control groups is due to the presence of defects in the phonological storage and recall of the articulatory loop of words especially the newly ones in the SLI children [23]. This explains the significant difference regarding the speech discrimination task. These results are in agreement with [24]. Regarding the speech discrimination (Table 2) the results agreed with other researchers who found a typical disorder of phonemic hearing (e.g., difficulties in distinguishing voiced from voiceless sounds) in SLI children. Most of SLI children are not able to recognize basic contents of the communication, to recognize key words essential for the communication contents [25]. In this study reduced P300 amplitude and prolonged latency (Table 2) in the SLI children are in agreement with [26], who also found the same findings even in the parents of SLI in tasks requiring a phonological discrimination. These parents had positive history of language delay. It was proposed that the prolonged P300 latency may represent a constitutional trait contributing to the language acquisition difficulties in SLI children [27], and their parents [26]. On studying the behavioral measures, long response time in the SLI group children, the ERP findings contribute these findings to a more detailed description of the processing [26]. This indicates that the long response time in SLI was not only a result of slow motor function. This is not trivial considering the many studies that have found poor motor skills in children with SLI [28]. The context updating hypothesis assumes that the elicitation of P300 reflects a process involved in the updating of representations in working memory. The updating of the memory representations of an event is assumed to facilitate the subsequent recall of that event. Finally the authors’ proposed that P300 amplitude is proportional to the degree of updating of the memory representations of the event [29]. P300 reflects updating of working memory [29], cognitive closure and transfer of information to consciousness [25]. P300 amplitude reflects the allocation of attention, while latency reflects speed of perceptual processing and classification [30]. Latency is a much more reliable indicator than amplitude being difficult to alter with attention [31]. Reduced amplitude may also reflect a shut off of later memory or attention evaluation of the discrepant stimuli analogous to the ‘‘optional’’ higher order processing [32]. The delayed latency hinted that more time was required to
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complete stimulus evaluation in the auditory modality at the higher processing level abnormally P300 is a reflection of abnormal functioning of neuronal generators (temporal, parietal and frontal areas), since these neuronal generators need to be intact for the P300 to attain normal levels [33]. The lack of significant correlation (Tables 3 and 4) between P300 latency and amplitude with all items under study within the control group disagree with [34] who gave evidence of age-related changes in P300 with decrease in latency and increase in amplitude from the age of 5 years until adult values are reached in late teens or early twenties. This can be explained by narrow age range in this study (from 4 to 6 years), thus age related changes are difficult to be obtained, and changes start at the age of 5 years and extend until adolescence. These results agreed with other researchers who found no evidence of any developmental change in children aged from 5 to 10 years. The highly significant correlation between P300 amplitude and chronological age can be explained by the delayed maturation theory and accordingly with the progress of age there is prolongation of amplitude but slower than in normal condition [35]. Our results indicate that with prolongation of P300 amplitude there will be improvement of expressive age (Table 3), verbal expression ability, grammatical closure, auditory sequential memory and sound blending (Table 4). This indicates the importance of memory and attention for the recording and recalling of large number of vocabulary and grammatical rules that are essential for the development of the previous items. The results also indicate that with increase of the speed of processing there is improvement of the expressive language age (Table 3), grammatical closure, auditory sequential memory, sound blending and auditory closure and speech discrimination (Table 4). These findings were consistent with other findings in suggesting impaired short-term auditory memory in those children [36]. The insignificant correlation of P300 amplitude and latency with auditory reception and association (Table 4) results disagreed with results of another study which concluded that SLI children have auditory processing deficit, not only in integration, but also in associative ability [37]. The results of this study agreed with the authors who suggested that the fundamental deficit in specific language impairment is a limitation in the brain capacity to rapidly process information [38]. Evidence for processing limitation is seen in studies showing that children with specific language impairment have longer response times associated with performing linguistic and non-linguistic tasks [26]. The smaller P300 amplitude in SLI group may represent less efficient context-updating in working memory. This would be in agreement with the theory put forth by [39] that involves a core deficit in short term memory due either to limited capacity in, or to more rapid decay from a short term store. Weakened memory representations could explain the performance of the language impaired children in this study. This may be explained by the prolonged perceptual processing in the SLI group, which may have resulted in a less distinctive memory event at the time for response decision, making the subject more uncertain about the status of the stimulus [40]. More complex grammatical structures may take longer to process than simpler structures. With increasing sentence complexity, structures that place greater demands on processing resources (such as grammatical inflections) may be omitted. Other factors that increase processing demands, such as phonologic complexity and even prosodic difficulty, can also impair comprehension and speech production in children with specific language impairment. Limitations in the amount of information that can be stored in verbal working memory may further constrain language processing [38].
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These findings are supported by authors who stated that: the potential link with language abilities is that all levels and forms of sensory memory are instrumental for consolidating transient stimulus traces into long-term representations during language acquisition, and later during language comprehension. Transient memories of stimulus occurrence may also contribute to neural processing of time, or ‘‘placing’’ events in time [41]. The whole previous results are consistent with the fact that auditory processing describes the way the brain assigns significance and meaning to the sounds in the environment. Effective auditory processing involves a relatively high speed of information transfer. It also requires a good attention span, a well-functioning memory, and sensitivity to the many subtleties of sound. When parts of this complex system break down or do not operate efficiently, listening is compromised. All the ensuing problems are collectively known as Auditory Processing Disorders (APD) [35]. 5. Recommendations - Further researches are needed to study more aspects of language by event related potential as N400 (an ERP that is sensitive to semantic aspects of the input). To clarify the role of phonological processing in more or less meaningful contexts and indicates a very early influence of the overall context on lexical processing in sentences. - These results should be taken in consideration during rehabilitation of the specific language impairment children.
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[32] L. Mottron, M. Dawson, I. Soulireres, B. Hubert, J. Burack, Enhanced perceptual functioning in autism and developmental disorders, J. Autism Dev. Disord. 36 (2006) 27–43. [33] M. Hoeksma, C. Kemner, J. Kenemans, H. Van England, Abnormal selective attention normalize P3 amplitude in developmental disorders, J. Autism Dev. Disord. 36 (2006) 643–656. [34] I. Shibasaki, S. Miyazaki, Event related potential in infant and children, J. Clin. Neurophysiol. 9 (1992) 408–418. [35] D.V.M. Bishop, R. Hardiman, W. von Suchodoletz, Atypical long-latency auditory event-related potentials in a subset of children with specific language impairment, Dev. Sci. 10 (5) (2007) 576–587. [36] J. Barry, M. Hardiman, E. Line, K. White, I. Yasin, D. Bishop, Duration of auditory sensory memory in parents of children with SLI: a mismatch negativity study, Brain Language 104 (1) (2008) 75–88. [37] O. Dlouha, Central auditory processing disorder in children with developmental dysphasia Oto-Rhino-Laryngology, in: Proceedings of the XVII World Congress of the International Federation of Oto-Rhino Laryngological Societies (IFOS) International Congress Series, vol. 1240, 2003, pp. 231–234. [38] J.W. Montgomery, Information processing and language comprehension in children with specific language impairment, Am. J. Speech Lang. Pathol. 22 (2002) 62–84. [39] S.E. Gathercole, A.D. Baddeley, Phonological memory deficits in language disordered children: is there a causal connection? J. Memory Lang. 29 (1990) 336–436. [40] M. Lahey, J. Edwards, Naming errors of children with specific language impairment, J. Speech Lang. Hear. Res. 42 (1999) 195–205. [41] R. Ceponiene, A. Cummings, B. Wulfeck, A. Ballantyne, J. Townsend, Spectral vs. Temporal Auditory Processing in Specific Language Impairment: A Developmental ERP Study. Project in Neural and Cognitive Development, University of California, San Diego, United States, 2009.
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Relation between language, audio–vocal psycholinguistic abilities and P300 in children having specific language impairment Elham Ahmed Shaheen a,*, Sahar Saad Shohdy a, Mahmoud Abd Al Raouf b, Shereen Mohamed El Abd c, Asmss Abd Elhamid a a b c
ENT Department, Phoniatric Unit, Faculty of Medicine, Cairo University, Egypt ENT Department, Faculty of Medicine, Cairo University, Egypt ENT Department, Audiology Unit, Faculty of Medicine, Cairo University, Egypt
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 April 2011 Received in revised form 1 June 2011 Accepted 2 June 2011 Available online 30 June 2011
Specific language impairment is a relatively common developmental condition in which a child fails to develop language at the typical rate despite normal general intellectual abilities, adequate exposure to language, and in the absence of hearing impairments, or neurological or psychiatric disorders. There is much controversy about the extent to which the auditory processing deficits are important in the genesis specific language impairment. The objective of this paper is to assess the higher cortical functions in children with specific language impairment, through assessing neurophysiological changes in order to correlate the results with the clinical picture of the patients to choose the proper rehabilitation training program. Subjects and method: This study was carried out on 40 children diagnosed to have specific language impairment and 20 normal children as a control group. All children were subjected to the assessment protocol applied in Kasr El-Aini hospital. They were also subjected to a language test (receptive, expressive and total language items), the audio–vocal items of Illinois test of psycholinguistic (auditory reception, auditory association, verbal expression, grammatical closure, auditory sequential memory and sound blending) as well as audiological assessment that included peripheral audiological and P300amplitude and latency assessment. The results revealed a highly significant difference in P300 amplitude and latency between specific language impairment group and control group. There is also strong correlations between P300 latency and the grammatical closure, auditory sequential memory and sound blending, while significant correlation between the P300 amplitude and auditory association and verbal expression. Conclusion: Children with specific language impairment, in spite of the normal peripheral hearing, have evidence of cognitive and central auditory processing defects as evidenced by P300 auditory event related potential in the form of prolonged latency which indicate a slow rate of processing and defective memory as evidenced by small amplitude. These findings affect cognitive and language development in specific language impairment children and should be considered during planning the intervention program. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Neurophysiology Illinois test P300 latency P300 amplitude Specific language impairment (SLI)
1. Introduction Language is a recent evolutionary phenomenon. In most children, the potential for language is present at birth [1]. Most children acquire language through environmental exposure to language without any special assistance. However, for some children with otherwise normal development, the acquisition of language proves
* Corresponding author at: ENT Department, Phoniatric Unit, Faculty of Medicine, Cairo University, 30 Milsa Towers, City Stars, Madinat Nasr, Cairo, Egypt. Tel.: +20 106423828; fax: +20 225319113. E-mail addresses: [email protected] (E.A. Shaheen), [email protected] (M. Abd Al Raouf), [email protected] (S. Mohamed El Abd), [email protected] (A. Abd Elhamid). 0165-5876/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2011.06.001
disproportionally difficult. Despite relatively normal nonlinguistic cognitive function and normal hearing, their language development is impaired. These children are considered to have specific language impairment (SLI) [2]. The failure of some children to master language at the normal rate has puzzled researchers for several decades. It was proposed that SLI is caused by low level auditory perceptual problems [3]. The criteria of diagnosis of specific language impairment that have been widely adopted either in part or in whole include a performance IQ (standard score) of at least 85 and at least one of the following: (a) a receptive language age (LA) score of at least 6 months below the mental age (MA) or chronological age (CA), whichever is lower; (b) a combined LA score of at least 12 months below the lower of MA or CA; or (c) an expressive LA score that is at least 12 months below the lower of MA or CA [4].
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Auditory information is translated by the sensory organs into neural activity, which in turn are processed and organized in the brain in different cortical and sub-cortical areas. In the thalamus, the information is processed and forwarded to the key cortical areas where more processing and integrating will take place [5]. The Auditory Brainstem Responses (ABR), measure the electrophysiologic activity from the 8th cranial nerve to the medial geniculate body of the brainstem [6]. Presentation of an auditory stimulus, such as a tone, triggers a sequence of neuronal events proceeding from the brainstem to cortex, reflection detection, classification, and interpretation of the sound. Late event related potentials (ERPs) can be used to index stage of auditory processing. P300 is the most used auditory event-related potential. This potential appears around 300 ms and requires attention, auditory discrimination and memory for its generation [7]. P300 has been considered an endogenous event related potential [8]. Endogenous responses depends both on the context within which the auditory stimuli are presented and attention of the subject [3]. It has been frequently claimed that children with specific language impairment have impaired central auditory processing, but there is much controversy about the role of such deficits in causing their language problems and it has been difficult to establish solid, replicable findings in this area. Insufficient attention has been paid to maturation aspects of auditory processing). The objective of this work is to assess the higher auditory cortical functions in children with specific language impairment, through assessing neurophysiological changes in order to correlate the results with the clinical picture of the patients to choose the proper rehabilitation training program. 2. Subjects and methods 60 pre-school Egyptian children were included in the study. Their ages ranged from 4 to 6 years, from the same socio-economic stratum. 40 children diagnosed as specific language impairment and 20 normal children to serve as a control group. The 2 groups were matched in age, gender and socioeconomic distribution. Consent was taken from the parents of all children participating in the study. Patient group consisted of 31 boys and 9 girls. Control group consisted of 16 boys and 4 girls. Testing the boys to girls difference was insignificant (chi 2 test = 0.95, P value > 0.05). Patient subjects meet the following criteria of specific language impairment [4]: 1 Normal peripheral hearing, 2 No neurological or psychological disorder, 3 No mental retardation, their intelligent quotient (IQ) is 90 or over (average), 4 Total language age is at least 12 months less than chronological age, and expressive language is at least 12 months less than the chronological age or the receptive language is at least 6 months less than the chronological age, control group criteria included: no history of delayed language development. Receptive, expressive and total language age matched their chronological age, normal development, and average IQ. All the participants were subjected to the language assessment protocol in the Phoniatric Unit, and to some neuro-physiological investigations applied in Audiology Unit, Kasr El Aini hospital in the period from 2006 to 2009, which included:
Examination: included: general, neurological, ear, nose and throat examination and preliminary language assessment. II Clinical diagnostic aids: 1 Arabic language test: This measures receptive age, expressive age, semantic age, pragmatic age and total language age [9] only receptive, expressive and total language age are included in this study. 2 Psychometric evaluation to measure the cognitive abilities: a Stanford Binet test 4th ed. [10] IQ = (mental age/chronological age) 100. b Illinois test of psycholinguistic abilities (ITPA) arabic edition [11] (2–10 years). In this study, only the audio–vocal items are studied which include: auditory reception, auditory association, verbal expression, grammatical closure, auditory sequential memory, auditory closure and sounds blending. The audio–vocal items can be arranged according to the structural complexity of items of the test as follows [12,13]: A Simple items: (knowledge dependent) auditory reception, verbal expression, grammatical closure, auditory association and auditory closure. B Complex items: (processing dependent) auditory sequential memory and sound blending. The test gives a psycholinguistic age and a diagnostic profile of psycholinguistic abilities. It also correlates highly with the childs intellectual abilities. It useful to assist in directing the remedial effort since it provides a profile or the abilities outlining the child particular strength and weaknesses. 3 Audiological assessment: i Pure tone audiometry, speech audiometry, immittancemetry, auditory brainstem response (ABR) [6] to confirm the normal peripheral hearing ability. ii Assessment of higher cognitive brain function using the event related potentials (ERP’s) namely auditory P300 amplitude and latency. Event related potential (P300): P300 was obtained with head phone TDH 39. An odd ball paradigm was used where the subject was instructed to react to occurrences of a tone (target) presented 20% of trials and to ignore a frequent tone present on other trials. P300 responses were obtained in response to the target stimuli. P300 amplitude: is the difference in microvolt between the point of maximum amplitude of the designated peak and stimulus baseline. P300 latency was measured from the time of stimulus onset to point of maximum amplitude of the chosen peak. Data were statistically described in terms of means standard deviation (SD), frequencies (number of cases) and percentages when appropriate. Comparison of quantitative variables between the study groups was done using Student t test for independent samples. For comparing categorical data, Chi square (x2) test was performed. Exact test was used instead when the expected frequency is less than 5 (Mont Carlo Exact method). Correlation between various variables was accomplished using Pearson moment correlation equation for linear relation. A probability value (P value) less than 0.05 was considered statistically significant. All statistical calculations were done using computer programs Microsoft Excel 2007 (Microsoft Corporation, NY, USA) and SPSS (Statistical Package for the Social Science; SPSS Inc., Chicago, IL, USA) version 15 for Microsoft Windows. 3. Results
I Elementary diagnostic procedures: Patient’s interview and history taking: including: personal, pre-natal, natal and post natal, developmental history, history of childhood illness and social behavior of the child.
Comparison of mean of chronological age between control group and children with SLI. The difference was insignificant. Chronological age of the control group ranged between of 4.40
E.A. Shaheen et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 1117–1122 Table 1 Comparison of the studied language items between the SLI cases and control group (Mont Carlo exact test). Item
SLI cases No.
Receptive language age 2–2.5 y 3 2.5–3 y 3–3.5 y 15 3.5–4 y 9 4–4.5 y 10 4.5–5 y 3 5–5.5 y 0 5.5–6 y 0 Expressive language age 2.5–3 y 6 3–3.5 y 15 3.5–4 y 16 4–4.5 y 1 4.5–5 y 2 5–5.5 y 0 Total language age 2 2.5–3 y 3–3.5 y 17 3.5–4 y 13 4–4.5 y 5 4.5–5 y 3 5–5.5 y 0
Control %
No.
%
7.5 37.5 22.5 25 7.5 0 0
0 0 0 6 3 9 2
0 0 0 30 15 45 10
15 37.5 40 2.5 5 0
0 0 0 5 11 4
0 0 0 25 55 20
5 42.5 32.5 12.5 7.5 0
0 0 0 6 8 6
0 0 0 30 40 30
Mont Carlo exact symbol significance
Table 2 Comparison between cases and controls regarding Illinois’ test of psycholinguistic abilities (audio–vocal items), P300 items and speech discrimination items under study. SLI cases (n = 40) Psycholinguistic items Auditory reception Auditory association Verbal expression grammatical closure Auditory sequential memory Auditory closure Sound blending Auditory items P300 amplitude P300 latency Speech discrimination
<0.001
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Controls (n = 20)
P value
3.45 0.52 3.23 0.41 3.36 0.50 3.08 0.51 2.68 0.41 3.23 0.44 3.45 0.41
4.86 0.55 4.71 0.53 4.92 0.61 4.92 0.63 4.77 0.70 4.79 0.73 4.65 0.85
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
8.65 1.79 365 29 81.78 3.39
12.73 1.12 278.4 27.9 91.70 2.43
<0.001 <0.001 <0.001
Data are represented as mean SD. Highly significant: P value < 0.001. SLI: specific language impairment. <0.001
<0.001
SLI: specific language impairment. %: is the percent within the group. Results revealed that there is a highly significant difference between the cases and the control group. The SLI group scored significantly lower than the control group in the receptive, expressive and total language age.
years and 5.80 years with a mean of 5.12 0.518 SD. Chronological age of the SLI group ranged between 4.11 years and 6.00 years with a mean of 5.24 0.618 SD, P value: 0.467 (P > 0.05). The results in (Table 1) revealed that there is a highly significant difference between the specific language impairment group and the control groups in the studied language items which included (receptive, expressive and total language age). The SLI group scored much lower than the control group. Table 2 revealed that the statistical comparison of the audio– vocal psycholinguistic items between the specific language impairment (SLI) and the control groups revealed highly significant differences in all items which included (auditory reception, auditory association, verbal excerption, manual excerptions auditory closure and auditory sequential memory). The SLI group scored much lower than the control group on comparing P300 amplitude and P300 latency is prolonged in SLI than in the control group. Speech discrimination item, the difference in all items is highly significant. Table 3 shows results of correlation within the SLI cases group revealed that there is a highly significant correlations between P300 amplitude with chronological, correlation of P300 amplitude
and latency with expressive language age are significant, correlations between P300 latency and amplitude with other items are insignificant. Within the control group, correlations between P300 amplitude as well as latency with chronological age as well as with language items under study are insignificant. Table 4 shows that within the SLI cases group, there is a significant correlation of P300 amplitude with auditory sequential memory while P300 latency has significant correlations with auditory closure and speech discrimination and a highly significant correlation with auditory sequential memory. Both P300 amplitude and latency have highly significant correlation with grammatical closure and sound blending. Otherwise correlations are insignificant. The correlations between the same items within the control group are insignificant. 4. Discussion In this study, P300 prolonged latency and small amplitude in the SLI group compared to the control group indicate the presence of higher cortical neurophysiological changes and late auditory perceptual processing stage deficit in these children. This means that there is slow processing of information and working memory defects that affected both language and cognition development. This can explain the low scores of the SLI children in both Language items and audio–vocal psycholinguistic items. This should be strongly considered in the construction of the rehabilitation program for SLI children. The significant difference in the receptive, expressive and total language age items between SLI children and control groups (Table 1) is explained by the poor general or the localized resource capacity theory of SLI children by [12]. These findings agreed with researchers
Table 3 Correlation between P300 amplitude and latency with chronological age and language items within each of SLI group and control group. Items
P300 amplitude Within group Correlation coefficient P value P300 latency Within group Correlation coefficient P value *
Chronological age
Receptive language age
Expressive language age
Total language age
SLI (40)
SLI (40)
SLI (40)
SLI (40)
0.601 0.001y
0.316 0.175
Control (20)
Control (20)
Control (20)
0.182 0.442
0.211 0.192
0.261 0.266
0.337 0.033*
0.398 0.082
0.274 0.088
0.248 0.292
0.212 0.370
0.296 0.206
0.096 0.68
0.510 0.021*
0.011 0.965
0.337 0.146
0.318 0.172
Means significant correlation (‘‘P’’ value < 0.05). Means highly significant correlation (‘‘P’’ value < 0.01). SLI: specific language impairment. y
Control (20)
0.095 0.690 0.489 0.029* 0.073 0.759 0.567 0.009y 0.122 0.608 0.504 0.023* 0.123 0.605 0.561 0.010y 0.153 0.519 0.574 0.008y 0.146 0.538 0.383 0.095 y
*
Means significant correlation (‘‘P’’ value < 0.05). Means highly significant correlation (‘‘P’’ value < 0.01). SLI: specific language impairment.
0.114 0.632 0.214 0.364 0.258 0.272
0.359 0.120
0.092 0.699 0.230 0.699 0.145 0.541 0.412 0.008y 0.289 0.217 0.267 0.096 0.203 0.390 0.339 0.033* 0.275 0.240 0.467 0.002z 0.316 0.175 0.438 0.005y 0.054 0.820 0.114 0.485 0.271 0.375
SLI Control SLI Control SLI Control SLI Control SLI Control SLI Control SLI Control SLI
0.271 0.091
P300 amplitude Within group Correlation coefficient P value P300 latency Within group Correlation coefficient P value
Sound blending Auditory closure Auditory sequential memory Grammatical closure Verbal expression Auditory association Auditory reception Items
Table 4 Correlation between P300 amplitude and latency and Illinois test of psycholinguistic abilities (audio–vocal items) and speech discrimination within each of SLI group and control group.
Control
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Speech discrimination
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who found that these children have fewer numbers of words to use spontaneously in expressing their ideas; they produce and comprehend fewer words than their normally developed peers [14]. The low auditory reception and auditory association ages in SLI children compared to the control group (Table 2) support the hypothesis of limitation of general resource receptive capacity in SLI children [15]. SLI children are slower in fast mapping and speed of processing of stimulus and need repeated exposure to the stimulus in to gain the meaning of the stimulus which leads to slow intake of language data from the input [16]. In this study, impaired auditory sequential memory in SLI children (Table 2) is in agreement with authors who used the complex memory span tasks [17]. Children with SLI showed marked deficits when the processing and storage demands of such tasks are verbal in nature [18], in non-word repetition task [19], and serial recall of digits and words [20]. The highly significantly low verbal expression and grammatical closure ages (Table 2) in the SLI compared to their control peers agreed with researchers who added that those SLI children may lack the basic vocal skills, and have inadequate vocabulary [21]. Our results are also in agreement with Pinke [22] who argued that domain-specific grammatical abilities develop from (genetic basis) pre-determined specialized mechanisms or neural circuitry provides evidence for the existence of a specialized grammatical subsystem in the brain, necessary for normal language development). In this study the low auditory closure and sound blending ages in the SLI group compared to control groups is due to the presence of defects in the phonological storage and recall of the articulatory loop of words especially the newly ones in the SLI children [23]. This explains the significant difference regarding the speech discrimination task. These results are in agreement with [24]. Regarding the speech discrimination (Table 2) the results agreed with other researchers who found a typical disorder of phonemic hearing (e.g., difficulties in distinguishing voiced from voiceless sounds) in SLI children. Most of SLI children are not able to recognize basic contents of the communication, to recognize key words essential for the communication contents [25]. In this study reduced P300 amplitude and prolonged latency (Table 2) in the SLI children are in agreement with [26], who also found the same findings even in the parents of SLI in tasks requiring a phonological discrimination. These parents had positive history of language delay. It was proposed that the prolonged P300 latency may represent a constitutional trait contributing to the language acquisition difficulties in SLI children [27], and their parents [26]. On studying the behavioral measures, long response time in the SLI group children, the ERP findings contribute these findings to a more detailed description of the processing [26]. This indicates that the long response time in SLI was not only a result of slow motor function. This is not trivial considering the many studies that have found poor motor skills in children with SLI [28]. The context updating hypothesis assumes that the elicitation of P300 reflects a process involved in the updating of representations in working memory. The updating of the memory representations of an event is assumed to facilitate the subsequent recall of that event. Finally the authors’ proposed that P300 amplitude is proportional to the degree of updating of the memory representations of the event [29]. P300 reflects updating of working memory [29], cognitive closure and transfer of information to consciousness [25]. P300 amplitude reflects the allocation of attention, while latency reflects speed of perceptual processing and classification [30]. Latency is a much more reliable indicator than amplitude being difficult to alter with attention [31]. Reduced amplitude may also reflect a shut off of later memory or attention evaluation of the discrepant stimuli analogous to the ‘‘optional’’ higher order processing [32]. The delayed latency hinted that more time was required to
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complete stimulus evaluation in the auditory modality at the higher processing level abnormally P300 is a reflection of abnormal functioning of neuronal generators (temporal, parietal and frontal areas), since these neuronal generators need to be intact for the P300 to attain normal levels [33]. The lack of significant correlation (Tables 3 and 4) between P300 latency and amplitude with all items under study within the control group disagree with [34] who gave evidence of age-related changes in P300 with decrease in latency and increase in amplitude from the age of 5 years until adult values are reached in late teens or early twenties. This can be explained by narrow age range in this study (from 4 to 6 years), thus age related changes are difficult to be obtained, and changes start at the age of 5 years and extend until adolescence. These results agreed with other researchers who found no evidence of any developmental change in children aged from 5 to 10 years. The highly significant correlation between P300 amplitude and chronological age can be explained by the delayed maturation theory and accordingly with the progress of age there is prolongation of amplitude but slower than in normal condition [35]. Our results indicate that with prolongation of P300 amplitude there will be improvement of expressive age (Table 3), verbal expression ability, grammatical closure, auditory sequential memory and sound blending (Table 4). This indicates the importance of memory and attention for the recording and recalling of large number of vocabulary and grammatical rules that are essential for the development of the previous items. The results also indicate that with increase of the speed of processing there is improvement of the expressive language age (Table 3), grammatical closure, auditory sequential memory, sound blending and auditory closure and speech discrimination (Table 4). These findings were consistent with other findings in suggesting impaired short-term auditory memory in those children [36]. The insignificant correlation of P300 amplitude and latency with auditory reception and association (Table 4) results disagreed with results of another study which concluded that SLI children have auditory processing deficit, not only in integration, but also in associative ability [37]. The results of this study agreed with the authors who suggested that the fundamental deficit in specific language impairment is a limitation in the brain capacity to rapidly process information [38]. Evidence for processing limitation is seen in studies showing that children with specific language impairment have longer response times associated with performing linguistic and non-linguistic tasks [26]. The smaller P300 amplitude in SLI group may represent less efficient context-updating in working memory. This would be in agreement with the theory put forth by [39] that involves a core deficit in short term memory due either to limited capacity in, or to more rapid decay from a short term store. Weakened memory representations could explain the performance of the language impaired children in this study. This may be explained by the prolonged perceptual processing in the SLI group, which may have resulted in a less distinctive memory event at the time for response decision, making the subject more uncertain about the status of the stimulus [40]. More complex grammatical structures may take longer to process than simpler structures. With increasing sentence complexity, structures that place greater demands on processing resources (such as grammatical inflections) may be omitted. Other factors that increase processing demands, such as phonologic complexity and even prosodic difficulty, can also impair comprehension and speech production in children with specific language impairment. Limitations in the amount of information that can be stored in verbal working memory may further constrain language processing [38].
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These findings are supported by authors who stated that: the potential link with language abilities is that all levels and forms of sensory memory are instrumental for consolidating transient stimulus traces into long-term representations during language acquisition, and later during language comprehension. Transient memories of stimulus occurrence may also contribute to neural processing of time, or ‘‘placing’’ events in time [41]. The whole previous results are consistent with the fact that auditory processing describes the way the brain assigns significance and meaning to the sounds in the environment. Effective auditory processing involves a relatively high speed of information transfer. It also requires a good attention span, a well-functioning memory, and sensitivity to the many subtleties of sound. When parts of this complex system break down or do not operate efficiently, listening is compromised. All the ensuing problems are collectively known as Auditory Processing Disorders (APD) [35]. 5. Recommendations - Further researches are needed to study more aspects of language by event related potential as N400 (an ERP that is sensitive to semantic aspects of the input). To clarify the role of phonological processing in more or less meaningful contexts and indicates a very early influence of the overall context on lexical processing in sentences. - These results should be taken in consideration during rehabilitation of the specific language impairment children.
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