Fostick, L., Babkoff, H., Zukerman, G. (accepted). Effect of 24 h of sleep deprivation on auditory and linguistic perception: A comparison with dyslexic readers and aging adults. Journal of Speech, Language, and Hearing Research. ***This is a self-archiving copy and does not fully replicate the published version*** Effect of 24 h of sleep deprivation on auditory and linguistic perception: A comparison among young controls, sleep deprived participants, dyslexic readers, and aging adults Leah Fostick*1, Harvey Babkoff2, and Gil Zukerman1 1 Department of Communication Disorders, Ariel University, Ariel, Israel 2 Department of Psychology, Ashkelon Academic College, Ashkelon, Israel Running Head: Sleep deprivation, auditory and linguistic percept *Corresponding author: Leah Fostick Department of Communication Disorders Ariel University, Ariel, Israel Tel. +972-54-4925354 Fax. +972-3-975-8908 [email protected] 1 Abstract Purpose. To test the effects of 24-hours of sleep deprivation on auditory and linguistic perception, and to assess the magnitude of this effect by comparing such performance to aging adults on speech perception, and to dyslexic readers on phonological awareness. Method. Fifty-five sleep deprived young adults were compared to 29 aging adults (above age 60), and to 18 young controls on auditory temporal order judgment (TOJ) and on speech perception tasks (Experiment 1). The sleep deprived were also compared to 51 dyslexic readers and to the young controls on TOJ and phonological awareness tasks (Reading non-words, Phoneme Deletion, Pig Latin, and Spoonerism) (Experiment 2). Results. Sleep deprivation resulted in longer TOJ thresholds, and poorer speech perception and non-word reading than the controls. The TOJ thresholds of the sleep deprived were comparable to the elderly, but their pattern of speech performance differed. They also performed better on TOJ and phonological awareness than dyslexic readers. Conclusions. A variety of linguistic skills are affected by sleep deprivation. The comparison of sleep deprived individuals with other groups having known difficulties in these linguistic skills might suggest that different groups might exhibit common difficulties. 2 Introduction Sleep deprivation has been known to affect human performance in several ways, including psychological, cognitive and motor performance (Babkoff, Caspy, Mikulincer, Sing, 1991a; Babkoff, Caspy, Mikulincer, 1991b; Dinges & Kribbs, 1991; Liberalesso, D’Andrea, Cordeiro, Zeigelboim, Marques, Jurkiewicz, 2012; Zukerman, Goldsteinm, Babkoff, 2007). The mechanisms by which sleep deprivation affects performance were hypothesized to be either general, i.e., by the tendency to fall asleep, physiologically, for short periods of time (i.e., microsleeps) while performing the tasks (The arousal theory, Babkoff et al., 1991a), or by more specific brain mechanisms, e.g., by affecting functions associated with the pre-frontal cortex (PFC) (Harrison & Horne, 2000a, 2000b), which theoretically could then have different effects on different cognitive functions (Babkoff, Goldstein, Zukerman, 2008; Harrison & Horne, 1998, 2000a, 2000b). For heuristic reasons, the majority of the studies of the effect of sleep deprivation on human performance, focused mainly on tasks and skills relating to human performance in daily life, particularly those required for shift work or other work-related demands (Babkoff et al., 2008). Very few of the earlier studies focused on the effect of sleep deprivation on auditory and linguistic perception. Auditory perception, especially auditory temporal processing, reflects the individual's ability to process series of auditory stimuli, presented rapidly. Several previous studies reported the negative impact of sleep deprivation on auditory temporal processing (Babkoff, Zukerman, Fostick, Ben-Artzi, 2005; Liberalesso et al., 2012). Following only 24-hours of continuous wakefulness, participants needed longer silent 3 intervals in order to discriminate two stimuli from one (Liberalesso et al., 2012), and needed longer inter-stimulus intervals (ISI) to correctly reproduce the order of two dichotic tones (Babkoff et al., 2005). One of the major implications of auditory processing to daily life is its putative relation to linguistic performance. A number of studies have reported a reduction in auditory temporal processing, and specifically temporal order judgment (TOJ) in different sub-populations that display linguistic difficulties. Among these populations are: 1) aphasic patients (Fink, Churan, Wittmann, 2006; von Steinbuchel, Wittmann, Strasburger, & Szelag, 1999); 2) young and adult dyslexic readers (Ben-Artzi, Fostick, Babkoff, 2005; Fostick, Bar-El, Ram-Tsur, 2012a,b; Reed, 1989; Tallal, 1980); 3) students with attention-deficit / hyperactivity disorder (ADHD) (Kleiner, Negbi, Or, Zuaretz, and Fostick, 2011); 4) and elderly individuals (Ben-Artzi, Babkoff, Fostick, 2011; Fink, Churan, Wittmann, 2005; Fitzgibbons and Gordon-Salant, 1998; Fostick & Babkoff, accepted; Szymaszek, Szelag, Sliwowska, 2006; Szymaszek, Sereda, Pöppel, Szelag, 2009). Reported effects of sleep deprivation on linguistic performance have been mixed. Earlier studies mainly tested verbal performance and articulation and found them to be negatively impacted by sleep deprivation (Harrison & Horne, 1998; Neville, Bison, French, & Boll, 1994; Schein, 1957). These findings are also supported by more recent studies (Bagnall, Dorrian, & Fletcher, 2011; Krajewski, Batliner, & Golz, 2009; Liu & Wissow, 2011; Orzeł-Gryglewska, 2010). However, the findings regarding other types of linguistic performance during sleep deprivation are relatively scarce and inconsistent. For example, speech comprehension was found to be affected by sleep deprivation in a recent 4 study (Pilcher et al., 2007) but not in an earlier study (Webb, 1986). Antonym identification was found to be affected by sleep deprivation in one study (word fluency, Harrison and Horne, 1998) but not in another (Pilcher et al., 2007). The different sub-populations of adults with diverse linguistic difficulties noted above (elderly, sleep deprived, dyslexic readers), all have been reported to show significant deficit in auditory temporal order judgments. Although these sub-populations share a difficulty in judgments of temporal order, they have distinct non overlapping linguistic profiles. The aim of the current study was, therefore, to test the effects of 24hours of sleep deprivation on auditory and linguistic perception. More specifically, we compared non sleep deprived with sleep deprived young adults on: 1) auditory dichotic temporal order judgments (TOJ); 2) speech perception; and 3) phonological awareness. Based on previous studies (Babkoff et al., 2005; Liberalesso et al., 2012), we hypothesize that TOJ thresholds will be longer during sleep deprivation. Since the literature reports a relationship between TOJ and various linguistic (dis)abilities, we also hypothesize that sleep deprivation will negatively impact speech perception and phonological awareness. In order to evaluate the expected decrease in these linguistic abilities, we compared the performance of the sleep deprived participants to that of two other sub populations: 1) aging adults (speech perception); and 2) dyslexic readers (phonological awareness). A common complaint among aging adults is difficulty in speech perception, especially when speech is rapid or when it is accompanied by a background noise (Humes et al., 2012; Schneider, Pichora-Fuller, Daneman, 2010, for a review). The elderly thus serve in the current study as a comparison group for difficulties in speech comprehension. Dyslexic readers have difficulties in acquiring reading skills and have 5 been shown to have deficit in phonological awareness, even as adults (Gabrieli, 2009, for a review). The dyslexic readers thus serve in the current study as a comparison group for difficulties in phonological awareness. As noted, both aging adults and dyslexic readers have longer TOJ thresholds, as compared to young adults (Fink et al., 2005; Humes, Kewley-Port, Fogerty, & Kinney, 2010; Szymaszek et al., 2006, 2009; Ben-Artzi et al., 2011) and normal readers (Ahissar, Protopapas, Reid, Merzenich, 2000; Ben-Artzi et al., 2005; Breier et al., 2001; Fostick et al., 2012a; Ramus et al., 2003; Reed, 1989; Tallal, 1980). Therefore, in order to evaluate the magnitude of the effect of sleep deprivation on auditory and linguistic perception, we report the results in two semi-overlapping experiments. Data for the sleep deprived (N=55) and for the control (N=18) participants are repeated in reports of Experiments 1 and 2. In Experiment 1, we report the: (a) TOJ thresholds and (b) performance on the speech perception tasks of the: 1) 24-hour sleep deprived young adults; 2) the non-sleep deprived aging adults (elderly); and 3) young non sleep-deprived, normal reading controls. In Experiment 2, we report the: (a) TOJ thresholds and (b) performance on the phonological awareness tasks of the: 1) 24-hour sleep deprived young adults; 2) the young dyslexic readers; and 3) young non sleepdeprived, normal reading controls. 6 Experiment 1: Speech perception TOJ deficit was reported both for sleep deprived young and healthy participants (Babkoff et al., 2005; Liberalesso et al., 2012) and for aging adults (Ben-Artzi et al., 2011; Fink et al., 2005; Fitzgibbons and Gordon-Salant, 1998; Fostick and Babkoff, 2013a; Szymaszek et al., 2006, 2009). Among aging adults, TOJ deficit, as part of the more general deficit in temporal resolution, has been associated with difficulties in speech perception (e.g., Humes et al., 2012; Schneider et al., 2010, for a review). However, to the best of our knowledge, this ability has not yet been tested among the sleep deprived. A few studies tested the effect of sleep deprivation on other linguistic abilities, such as speech comprehension (e.g., Pilcher et al., 2007; Webb, 1986) but the reported results were not clear. The aim of the current study was, therefore, to test the effect of 24-hours sleep deprivation on the ability to correctly identify spoken words. A second aim of the current study was to estimate the magnitude and significance of the effect of sleep deprivation on speech perception. A large number of studies have documented the difficulties that aging adults have with speech perception, under different conditions (see, e.g., Humes et al., 2012, for a review of different speech perception tasks). Therefore, the aim of Experiment 1 was to compare the speech perception of sleep deprived participants to that of aging adults. Moreover, we wished to replicate the findings of TOJ deficit among the sleep deprived and aging adults that was previously reported in order to have a basis of comparison of the sleep deprived with the elderly. Consequently, we also compared TOJ thresholds of the sleep deprived and aging adults to those of non-sleep deprived young participants. 7 Finally, in an attempt to evaluate the relationship between TOJ and speech perception, correlation analyses were carried out between TOJ and speech perception tasks, for all participants and for each group separately. In order to use a full betweensubjects design, the performance of the experimental groups (i.e., sleep deprived and aging adults) was compared to non-sleep deprived, young, normal reading participants, (a procedure similar to Harrison and Horne (1998) and Tucker, Stern, Basner, & Rakitin, 2011). Method Participants The study included 102 participants, 55 sleep deprived young adults, 29 aging adults, and 18 young adult non sleep deprived students with no learning difficulties, who served as a control group. All participants were screened for normal hearing on 500, 1,000, 2,000, and 4,000 Hz, and were native Hebrew speakers. Young participants (sleep deprived and control groups) had hearing thresholds ≤ 0 dB HL. Elderly participants had hearing thresholds ≤ 15 dB HL. All participants had less than 5 dB threshold differences between ears. See Table 1 for the demographic data for all participants. Tasks and stimuli Auditory TOJ was measured using the dichotic TOJ task (see also Babkoff et al., 2005; Ben-Artzi et al., 2011; Ben-Artzi et al., 2005; Fostick and Babkoff, 2013a,b; Fostick et al., 2012a,b; Fostick, Ben-Artzi, Babkoff, 2011). Although all participants had hearing 8 levels within their age-norms, in order to avoid possible effect of differences in hearing thresholds, the auditory stimuli were delivered at the same sensation level (40dB SL) for all the participants. Therefore, before participants performed the TOJ task, an absolute threshold task was performed using the same equipment and experimental conditions as in the TOJ task. The hearing threshold was measured for 1kHz 15 msec tones using a two alternative forced choice 2-down-1-up adaptive staircase procedure. Hearing threshold was calculated as the average of the last eight out of 10 reversals. Threshold values were converted to dB SPL using TA 1350A Sound Level Meter. Table 1 presents hearing threshold data for the study tone. The individual's hearing threshold was entered into the program which then delivered the tones for the TOJ task at 40 dB SL. In the TOJ task, the participants were required to reproduce the order of two identical tones delivered each to a different ear (participants' responses were either rightleft or left-right). Both stimuli were 15 msec 1 kHz pure tones which were presented at 40 dB SL, with 1 msec cosine-squared rise/fall envelopes on each trial. The tone pairs were presented with an inter-stimulus interval (ISI) of either 5, 10, 15, 30, 60, 90, 120 or 240 msec separating them. On half of the trials, the order of the presentation of the tones was left ear first followed by the right ear and in the reverse order on the other half of the trials. Participants pressed the relevant keyboard keys in the order corresponding to what they heard. Each ISI value was repeated 16 times, resulting in a total of 32 trials for the current analysis. TOJ threshold was calculated as the ISI needed for 75% correct responses. Experimentation followed four training phases (see also Ben Artzi et al., 2005; Fostick & Babkoff, accepted). In the first training phase, participants were familiarized 9 with the stimuli used in the study by listening to five tones in the right ear followed by five tones in the left ear. In the second phase, the participants were trained to associate each tone with the proper response key in 32 trials in each they were required to press the correct key for each tone they heard. Feedback was given following each response (“right” or “wrong”). In the third phase, the participants were tested for the ear-key association and were required to press the correct key for each tone, but without any feedback, in order to ensure that the participants associated correctly between the ear of the tone and the correct keyboard response key. All participants passed this phase successfully with at least 20 correct trials out of 24. In the fourth phase, participants were trained to reproduce the order of two tones. This phase was similar to the conditions of the experiment, but with an ISI = 240 mesc and with only 32 trials. Performance in this phase was accompanied by appropriate feedback after each response (“right” or “wrong”). Both the absolute threshold and TOJ tasks were computed using MatLab software which delivered the sounds and recorded the responses. Sounds were delivered using TDH-49 headphones. Speech perception was tested using the Hebrew version of the AB words test (Boothroyd, 1984). The test is composed of lists of ten one-syllable Consonant-VowelConsonant meaningful words, which are phonemically balanced (i.e., in each list every consonant appears once and every vowel appears twice). The words were presented binaurally and the participants were required to repeat each word immediately after hearing it. 10 The words were presented in four conditions, speech perception in: 1) quiet; 2) speech noise; 3) white noise; 4) and compressed speech at a 60% compression rate. Two lists (20 words) were used in each condition and three seconds separated each word. The words were edited using the SoundForge program which digitized (16-bit) at a sampling rate of 44kHz. The words level was normalized using the overall RMS. In the quiet condition, words were presented with no background noise. In the speech noise condition, words were accompanied by background broadband noise composed of steady-state frequencies within the range of 0.5-2kHz (band-passed noise). In the white noise condition words were accompanied by wide-band white noise which was evenly distributed over the entire range of frequencies (.25-8kHz). Speech and white noise were generated from the Diagnostic Audiometer DA64 and had identical spectrotemporal features on every trial. They were added to the words at an SNR of 0 dB. The noise started three seconds before the first word in the list and continued non-stop through the list, ending with the last word. In quiet, SpN, and WN conditions words were presented at a rate of 120 wpm. In the 60% compressed speech condition, words were compressed to be 60% of their original length, and were presented with no background noise at a rate of about 200 wpm with the same three seconds of silent interval between them. The compression was carried out using an implementation of the WSOLA (Waveform Similarity Overlap and Add) algorithm (Verhelst, 2000) which achieves very high quality time-scale modification of speech signals while maintaining other qualities, such as the pitch and the timbre, unchanged. 11 Procedure The study was approved by the ethics Institution Review Board (IRB) and is in accordance with Good Clinical Practice (GCP) guidelines. All participants received full explanation about the study and signed an informed consent. Screening for hearing sensitivity was done prior participation in the study. Sleep deprived participants signed the informed consent and had the hearing sensitivity screening before the sleep deprivation night. Sleep deprived participants were tested following at least 24-hours of no sleep (mean=25 hours, s.d=.5). The night before experimentation was spent at home. Until the evening, all participants were engaged in academic activities. Between 9:00PM and 6:00AM they phoned the laboratory every 20 minutes and left a message verifying that they are awake. The participants were instructed to refrain from physical exercises, as well as from smoking or ingesting any foods or beverages that contained caffeine or alcohol, during the day before experimentation. Following the sleep-deprived night, participants came to the laboratory and performed the study tasks as described in Experiments 1 and 2. Results The rationale for measuring speech perception among the sleep deprived, and comparing them to aging adults, derives from earlier research that reported increased TOJ thresholds both for the elderly and for the sleep deprived. Therefore, we first compared the TOJ thresholds of the sleep deprived and the aging adults to the control group (Figure 1). 12 Analysis of variance (ANOVA) indicated a significant effect for group (F(2,88)=4.87, p<.01, partial eta squared=.21). Fisher’s least significant difference (LSD) post hoc test showed that the dichotic TOJ thresholds of the control group are significantly shorter than the sleep deprived (p<.05, Cohen's d=.53) and the elderly (p<.01, Cohen's d=.94), but no difference in mean TOJ threshold was found between sleep deprived and aging adults (p>.05, Cohen's d=.11). Speech perception data for sleep deprived young adults, the elderly and young controls are presented in Table 2. Hearing thresholds were treated as a covariate in the analyses of speech perception. The variance of speech perception data differed significantly among the three groups for the quiet, SpN, and 60% compression conditions (see Table 2). Therefore, speech perception data for these conditions were transformed using arcsine transformation. Following this transformation, no differences in variances among study groups were found in any of the speech perception conditions (F(2,89)=.54 to .73, p>.05). Significant group effects were found in: 1) speech perception in SpN; 2) speech perception in WN; and 3) when speech is 60% compressed (Table 2). No differences among groups were found for speech perception in quiet. Fisher’s LSD post hoc test on the arcsine-transformed data for quiet, SpN, and 60% compression conditions and for raw data in the WN condition, indicated that speech perception for the sleep deprived group was significantly lower than for the young controls in: 1) the SpN condition (p<.01, Cohen's d=.75); 2) the WN condition (p<.01, Cohen's d=.74), and 3) when speech was 60% compressed (p<.001, Cohen's d=.68). In addition, speech perception for the sleep deprived was significantly lower than for the 13 elderly in 1) the WN (p<.05, Cohen's d=.66) and 2) 60% compression (p<.001, Cohen's d=.84) conditions. However, in the SpN condition, speech perception by the sleep deprived was significantly better than for the elderly (p<.01, Cohen's d=.66). Pearson correlation between TOJ thresholds and the speech perception tasks including all the participants, revealed a significant correlation only with speech perception in SpN (r=-.25, p<.05). Testing the correlation between TOJ and speech perception tasks separately for each group revealed again only significant correlation between TOJ and speech perception in SpN, and only for the sleep deprived (r=-.34, p<.05). Discussion Consistent with previous studies, both sleep deprived and aging adults had longer TOJ thresholds, than the non-sleep deprived controls. Interestingly, there was no difference between the TOJ thresholds of the sleep deprived and the elderly. A similar trend of comparable performance between sleep deprived young adults and aging adults was previously reported by a number of researchers (Durmer & Dinges, 2005; Harrison, Horne, & Rothwell, 2000; Muzur, Pace-Schott, & Hobson, 2002; Tucker et al., 2011) using a variety of different tasks. Harrison et al. (2000) argued that both aging adults and sleep deprived young adults have similar disruptions in the prefrontal cortex and similar patterns of response when executive functions are measured. They even suggested that sleep deprivation can be viewed as a model for healthy aging. As hypothesized, sleep deprivation had a negative effect on speech perception as indicated by the lower accuracy scores of the sleep deprived under all conditions of 14 speech perception except for speech perception in the quiet baseline condition. Apparently, speech perception is impacted by sleep deprivation similar to other linguistic abilities that have been reported to be affected negatively be sleep deprivation (e.g., Harrison and Horne, 1998; Pilcher et al., 2007). Contrary to the TOJ findings, which showed similar performance of sleep deprived young adults and aging adults, the comparison between the sleep deprived and aging adults on the speech perception tasks yielded a different and more complex picture. Important to note (see Table 4) is the difference in response pattern among these groups, as no one group was consistently better or worse than the other group under all speech perception conditions. The sleep deprived were better than the elderly in speech perception in the SpN condition, but performed poorer in the WN and 60% speech compression conditions. The correlations between TOJ and speech perception were significant only for the SpN condition when all participants were included. However, when the correlations were tested for each group separately, only the correlation for the sleep deprived was significant. We had expected a significant association between TOJ and speech perception under the SpN based on earlier studies that showed a significant relationship between speech perception and temporal resolution (Fostick, Ben-Artzi, & Babkoff, accepted; Snell and Frisina, 2000; Snell, Mapes, Hickman, & Frisina, 2002). A lack of such relationship in the control group may be due to a ceiling effect, as well as the small variance. However, it was surprising that no correlation between TOJ and speech perception was found for the elderly. It may be that by splitting the participants into young and elderly we found group differences, but reduced the age variability which 15 caused range restriction. In addition, testing each group separately reduced the number of participants in each group. The results that showed different response patterns of sleep deprived participants, as compared to the elderly do not support the claim of Harrison et al. (2000) that sleep deprivation may serve as a model for healthy aging and may suggest, instead, that speech perception mechanisms are impacted differently by aging than by sleep deprivation. In fact, Tucker et al. (2011) suggested that sleep deprivation and aging might affect the same mechanisms differently (the "double dissociation" theory). They showed that although some of the global performance was affected similarly by sleep deprivation and aging (i.e., reaction time and time between the response to the next stimuli), some types of performance were affected only by aging (e.g., working memory scanning speed) and some only by sleep deprivation (e.g., vigilance and non-executive processes such as response selection and psychomotor reaction). In comparing the performance of sleep deprived young adults and aging adults on speech perception, one should recall that the sleep deprived may suffer from decreased attention or vigilance but not from auditory deficit, e.g., decreased hearing sensitivity. In contrast, the elderly likely have decreased hearing sensitivity and possibly some decrease in cognitive performance as well as in perceptual processes. All of the above enumerated changes from the norm in the control condition may affect speech perception negatively, but each type of deficit may affect speech perception in a different manner and to a different extent. For example, let us compare the impact of hearing loss among the elderly in speech perception in the two noise conditions: 1) speech masked by white noise; and 2) speech masked by speech noise (SpN). In the SpN condition, words were 16 masked by background noise composed of steady-state frequencies within the range of 0.5-2kHz (band-passed noise). In the white noise condition words were masked by wideband white noise which was evenly distributed over the entire range of frequencies (.258kHz). Age-related decreases in hearing sensitivity are mainly related to high frequencies, with some loss in the mid-frequency range and much less loss in the low frequency range. In the white noise condition (in which noise energy is evenly spread along the audible spectrum, including both high and low frequencies), the age-related decrease in high frequency hearing thresholds might have had a smaller impact since the low frequencies in the test words are relatively less masked. However, in the SpN condition, the noise energy is mainly concentrated in the low to mid-frequency spectrum thus resulting in relatively greater masking of the low-to-mid range frequency of the words. We suggest that the combination of noise masking in the low-mid frequencies and (probable) elevated thresholds in the high frequency range might contribute to the much poorer performance by the elderly as compared to the sleep deprived in the speech in SpN condition. Support for this hypothesis may be seen by comparing the differences between aging adults and the control group versus the differences between the sleep deprived and the control group, on the various speech perception tasks. While the magnitude of the difference between the sleep deprived and the control participants appears consistent across speech perception tasks, the magnitude of the difference between aging adults and the controls differs across tasks. These results may provide support of vigilance/attention factor for the sleep-deprived group that impacts performance across 17 all tasks, while a different factor, such as hearing sensitivity, appears to impact the performance of the elderly. 18 Experiment 2: Phonological awareness The rationale for testing the effects of sleep deprivation on phonological awareness was derived from previous studies that reported increased TOJ thresholds in both sleep deprived young- healthy participants (Babkoff et al., 2005; Liberalesso et al., 2012) and dyslexic readers (Ben-Artzi et al., 2005; Fostick et al., 2012a,b; Reed, 1989; Tallal, 1980). The auditory temporal discrimination deficit found among dyslexics has been understood by some researchers to be related to their reading and phonological difficulties (Ben-Artzi et al., 2005; Fostick et al., 2012b; Tallal, 1980). Regarding the sleep deprived, phonological awareness has not yet been studied, to the best of our knowledge. Word fluency, verbal performance and articulation were previously tested and found to be negatively affected by sleep deprivation in some studies (e.g., Harrison & Horne, 1998; Pilcher et al., 2007) but not in all (e.g., Pilcher et al., 2007; Webb, 1986). The first aim of Experiment 2 was therefore, to test the effects of 24-hours of sleep deprivation on the ability to perceive and manipulate speech sounds, i.e., phonological awareness. A second aim was to estimate the magnitude and significance of the effect of sleep deprivation on phonological awareness. Therefore, in Experiment 2 we compared sleep deprived participants' phonological awareness to that of dyslexic readers. Moreover, in order to replicate and compare the reported increased TOJ thresholds among both sleep deprived and dyslexic readers, we first compared TOJ thresholds for these groups with the non-sleep deprived control participants. Furthermore, we tested the 19 correlations between TOJ thresholds and the phonological awareness tasks for all participants together and for each group separately. As in Experiment 1, the performance of the participants in both experimental groups (i.e., sleep deprived and dyslexic readers) was compared to non-sleep deprived, young, normal reading participants, in order to use a full between-subjects design (similar design used by Harrison and Horne, 1998; and Tucker et al., 2011). Method Participants The same 55 sleep deprived young adults and 18 young adult students (described in Experiment 1) were included in the current study. In addition, 51 Hebrew speaking dyslexic readers, with normal hearing (≤0 dB HL), participated in the study. These participants had prior professional diagnosis of dyslexia and were only included in the study if: 1) they were at least one standard deviation below the mean for the Shatil (1995a) reading regular words test (see also Fostick et al., 2012a,b); and 2) had a score equal to or higher than the 25th percentile on the Matrices subtest of the Wechsler Adult Intelligence Scale (WAIS) (Wechsler, 1997). Participants with a diagnosis of attention disorder /hyperactive disorder (ADHD) or other learning disabilities (such as dysgraphia) were not included in the study. See Table 1 for the demographic data of all participants. 20 Tasks and stimuli Auditory TOJ was measured using the dichotic TOJ task that was described in Experiment 1, along with the measurement of absolute threshold to insure similar sensation levels for all participants. Reading non-words (Shatil, 1995b). This task was designed to measure the amount of non-words per minute read correctly by the participant. The participant was presented with a list of 86 solitary dotted (pointed) non-words (full Hebrew vowel diacritics), creating high orthographic richness with a high spelling-to-sound correspondence (Frost, 1994). Each participant was asked to read the words as fast and as correctly as possible for one minute. The score reflects the number of words per minute the participant read correctly. Phoneme Deletion (Share, 1997). This test included 20 Hebrew meaningful words that were read aloud by the experimenter. After each word, the participant was instructed to repeat the word while omitting one of the phonemes which then resulted in a non-word (e.g., to say the word MASMER – Hebrew word for nail – without the sound 'S', which is MA-MER). The place of the omitted phoneme was changed (beginning, middle or end of word), creating different levels of difficulty in performing the task. Accuracy level reflects the participants' score on this task. Pig Latin (Shatil, 1995c). This test included six Hebrew non-words that were read aloud by the experimenter. After each word, the participant was instructed to repeat it while pronouncing the first phoneme at the end of the word and adding the vowel /a/ which also resulted in a non-word (e.g., the non-word 'VIK' becomes 'IKVA'). Accuracy level reflects the participants' score on this task. 21 Spoonerism (Shatil, 1995d). This test included six pairs of Hebrew words that were read aloud by the experimenter. After each pair the participant was instructed to repeat them while switching the first phoneme of the two words which results in both words becoming non-words. Accuracy level reflects the participants' score on this task. Procedure Measuring TOJ thresholds and phonological awareness among the sleep deprived, dyslexic readers, and control group participants was approved by the ethics Institution Review Board (IRB). All procedures are in accord with Good Clinical Practice (GCP) guidelines. The participants received full explanations about the study, and signed an informed consent form. Screening for hearing sensitivity was performed prior to participation in the study. Results Note Fig. 1 for the mean dichotic TOJ thresholds and standard deviations for all study groups in Experiments 1 and 2. TOJ threshold variance differed significantly among the control group, the sleep deprived and the dyslexic readers (F(2,101)=9.33,p<.001). Consequently, the data were log-transformed. Following the log transform, no differences in TOJ threshold variances were found (F(2,101)=.51, p>.05). Analysis of variance (ANOVA) carried out on the transformed TOJ thresholds indicated a significant effect for group (F(2,104)=11.76, p<.001, partial eta squared=.28). The order of the dichotic TOJ thresholds is shown in Figure 1 from the shortest (control group, left-most) to the longest (dyslexic group, right-most). Fisher’s least significant difference (LSD) post hoc test 22 showed that the dichotic TOJ thresholds of the sleep deprived were significantly longer than the control group (p<.05, Cohen's d=.53) and significantly shorter than the dyslexic readers’ (p<.001, Cohen's d=1.26). Phonological awareness data for sleep deprived young adults, dyslexic readers, and young controls are presented in Table 3. The variance of phonological awareness scores in all tasks differed significantly among the groups (Table 3). Therefore, the data for all phonological awareness tasks were transformed using arcsine transformation. Following the data transformation, no differences in variances among study groups were found in any of the phonological awareness tasks (F(2,109)=1.19 to 2.76, p>.05). Significant group effects were found in all of the phonological awareness tasks (Table 3). Fisher’s LSD post hoc test on the arcsine-transformed data, revealed that the sleep deprived did not differ from the controls on any of the phonological tasks except for nonword reading, in which the young controls had significantly higher scores than the sleep deprived (p<.001, Cohen's d=1.40). When compared to dyslexic readers, the sleep deprived had higher scores on all of the phonological awareness tasks (non-words, p<.001, Cohen's d=.79; phoneme deletion, p<.001, Cohen's d=1.36; Pig Latin, p<.01, Cohen's d=.90; Spoonerism, p<.01, Cohen's d=.74). Pearson correlation between TOJ and phonological awareness tasks that included all of the participants indicated significant correlations for all measures (Table 3). Separate analyses for each group revealed significant correlations among the sleep deprived between the TOJ thresholds and phoneme deletion accuracy (r=-.31, p<.05). Among the dyslexic readers significant correlations were found between TOJ threshold and non-word reading (r=-.42, p<.05), Spoonerism (r=-.37, p<.05), and Pig Latin (r=-.32, 23 p<.05) tasks. No correlations between TOJ thresholds and any of the phoneme awareness tasks were found for the control group. Discussion In accord with previous findings, both the sleep deprived and dyslexic readers had longer TOJ thresholds than control participants. However, the TOJ thresholds of the sleep deprived were also significantly shorter than those of the dyslexic readers. Thus, the effect of 24 hours of sleep deprivation on auditory TOJ was smaller than the effect of dyslexia. Sleep deprivation had a negative impact on non-word reading but not on the other phonological awareness tasks. In addition, significant correlations between TOJ and phonological awareness tasks were found both for the sleep deprived and for dyslexic readers, but in different tasks. These mixed results are similar to the general findings in the literature regarding the effect of sleep deprivation on different linguistic tasks, in which some studies report poorer performance among the sleep deprived (Bagnall et al., 2011; Harrison & Horne, 1998; Krajewski et al., 2009; Liu & Wissow, 2011; Neville et al., 1994; Orzeł-Gryglewska, 2010; Schein, 1957) while others do not find such an effect (e.g., Pilcher et al., 2007). The mixed results for the sleep deprived may be related to differences in the way the phonological awareness tasks were performed as well as in task difficulty. For example, most of the phonological awareness tasks used in the current study (namely, phoneme deletion, Pig Latin, and Spoonerism) were tasks that involved continuous interaction with the experimenters who read the initial words and sounds that the 24 participants needed to manipulate. For these tasks there was no negative impact of sleep deprivation. The only phonological awareness task that required the participant to perform by him/herself from beginning to end was the non-word reading task in which performance of the sleep deprived was lower than of the non-sleep deprived controls. Perhaps the lack of interaction with an experimenter during the performance of this task allowed the effect of decreased attention or vigilance (due to sleep loss) to predominate. The sleep deprived were better than the dyslexic readers on TOJ thresholds and also on all phonological awareness tasks. A number of studies have reported significant relationships between TOJ and phonologic abilities (Ben-Artzi et al., 2005; Fostick et al., 2012b). Consequently, we expected better performance in phonological awareness tasks by the sleep deprived than by the dyslexic readers, since the former have shorter TOJ thresholds than the latter. However, we also expected better performance by the nonsleep deprived controls than the sleep deprived on all of the phonological awareness tasks since sleep deprivations impacts negatively on TOJ thresholds. The results of the current study do not completely conform to this prediction. The performance of the sleep deprived and the control group was similar on all phonological tasks, except for the nonword reading task. Similar results were also found in another study from our lab that used a within-subjects design for sleep deprivation (Zukerman, & Fostick, 2010). Perhaps the difference between sleep deprived young adults and dyslexic readers in terms of the magnitude of TOJ deficit can account for the difference in performance on the phonological awareness test between these groups, even if we assume a strong relationship between TOJ thresholds and phonological awareness. While sleep deprived young adults had 42% longer TOJ thresholds, than the non-sleep deprived controls, the 25 dyslexic readers’ TOJ thresholds were 141%, longer than the controls. Perhaps the relatively small deficit in TOJ as found in the sleep deprived does not affect phonological awareness as extensively as the substantial deficit found in the group of dyslexic readers. Alternatively, these findings might suggest that different mechanisms are affected by dyslexia than by sleep deprivation and therefore affect auditory and linguistic perception in dyslexia differently than in sleep deprivation. Sleep deprivation is certainly no model for dyslexia. 26 General Discussion The purpose of the current study was to test the effects of 24-hours of sleep deprivation on auditory and linguistic perception, and to assess the magnitude of this effect by comparing the deficit with the performance of aging adults and dyslexic readers, who are known to have linguistic difficulties. In support of our hypothesis, the data indicate that 24-hours of sleep deprivation resulted in longer TOJ thresholds and lower scores on three speech perception conditions and one of four phonological awareness tests (non-word reading). The comparison of a group of sleep deprived individuals with young non sleep deprived controls and other groups of individuals who are also reported to have TOJ deficit and language difficulties, namely aging adults (speech comprehension) and dyslexic readers (phonological awareness), is summarized in Table 4. The pattern of difficulties in speech perception among sleep deprived young adults was different from that of aging adults, even though their TOJ threshold performance was comparable. With regard to the sleep deprivation-dyslexic comparison, sleep deprived participants performed better than dyslexic readers on all of the phonological awareness tasks as well as on TOJ threshold. Sleep deprived participants only performed more poorly that the controls on the non-word reading task. It was suggested previously (Harrison et al. (2000) that sleep deprivation among young adults can be regarded as a model for healthy aging. However, the results of the current study cannot support such an argument. Although both the elderly and sleep deprived had more elevated TOJ thresholds than the control group and did not differ from each other, nevertheless, the performance pattern of the elderly and the sleep deprived 27 differed on the speech perception tasks. These results support the previously mentioned "double dissociation" theory (Tucker et al., 2011), and suggest that different mechanisms are involved in the speech perception performance of sleep deprived and aging adults. In the present study, aging adults and dyslexic readers were considered as comparison groups to assess the effects of sleep deprivation on auditory and linguistic processing. However, having both groups in one study raises interesting possibilities regarding the possible comparison between the two groups. On the one hand, dyslexia and aging are different both in nature and in performance deficits. While dyslexia runs in families, has a genetic basis, is usually diagnosed at childhood, and persists into adulthood (e.g., Peterson & Pennington, 2012), the effects of aging emerge only when the individual has reached and passed his/her optimum performance levels (see e.g., Humes et al., 2012; Rabbit, Diggle, Holland, & McInnes, 2004; Salthouse, 2011). While dyslexia is defined solely with the difficulty in acquiring reading skills, the linguistic difficulty of aging adults has been reported to be related to speech perception. Therefore, it seems that these two conditions have no common basis. On the other hand, both conditions are characterized by TOJ deficit, although with quite different magnitudes, as was shown in the current study. As TOJ deficit has been reported to be related both to speech perception and to phonological awareness (e.g., Ben-Artzi et al., 2005; Fostick et al., 2012b; Gordon-Salant and Fitzgibbons, 1993; Schneider, Pichora-Fuller, Kowalchuk, & Lamb, 1994; Snell et al, 2002), one can legitimately ask whether the two groups have deficits in reading and phonological skills and speech perception. This question was not tested in the current study, but some recent studies point to a possible deficit in speech perception among dyslexic readers (Boets, Wouters, van Wieringen, & Ghesquière, 2011; 28 Bruder et al., 2011; Fostick & Korecky, Maltz, Babkoff, 2012; Ziegler, Pech-Georgel, George, & Lorenzi, 2009) and to some extent to poor phonological awareness among aging adults (Fostick and Babkoff, 2011). The implications of the current study are twofold. First, the finding that speech perception and some phonological awareness abilities are significantly affected by sleep deprivation is important clinically for people who work under sleep deprivation or sleep restricted conditions, especially if their work and service depend on good receptive language abilities. Since no effect of sleep deprivation on speech perception in quiet was found, the data suggest that it is worthwhile to maintain optimal speech perception conditions for those whose work is often accompanied by sleep loss. Second, in the current study we found that although sleep deprived young adults had auditory TOJ deficit, their linguistic difficulties were different from those of other groups with similar TOJ deficit, namely aging adults and dyslexic readers. These results also suggest that the relationship between TOJ and linguistic abilities may only be partial and that additional factors affect linguistic performance. 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Demographic data for study participants Sex Females Age Hearing thresholds, 1kHZ pure tone (dB SPL) Males Mean (SD) Minimum Maximum Mean (SD) Minimum Maximum Sleep deprived 30 (55%) 25 (45%) 23.60 (1.93) 20 28 18.4 dB (.05) 15 dB 20 dB Control 5 (28%) 13 (72%) 25.61 (3.31) 21 31 18.7 dB (.1) 15 dB 20 dB Aging adults 16 (55%) 13 (45%) 68 (6.55) 60 82 32.4 dB (1.96) 15 dB 35 dB Dyslexic readers 19 (37%) 32 (63%) 26.57 (4.18) 19 40 18.6 dB (.08) 15 dB 20 dB 39 Table 2. Mean percent correct (SD) for speech perception in four conditions for study groups, Levene test, and one-way ANCOVA between groups (partial Etta Squared), controlling for hearing thresholds Sleep deprived Young controls Aging adults Levene Statistic F Quiet 98% (3%) 98% (4%) 98% (6%) 3.18* .32 (.02)1 SpN 87% (8%) 92% (5%) 81% (10%) 5.07** 12.44*** (.39)1 WN 65% (10%) 72% (9%) 70% (9%) .30 6.53** (.32) 60% Compression 91% (6%) 96% (2%) 95% (3%) 4.51* 13.75*** (.46)1 1 For arcsine-transformed data **p<.01; ***p<.001 40 Table 3. Mean percent correct (SD) for phonological awareness tasks, and one-way ANOVA (partial eta Squared) between study groups. Sleep deprived Young controls Dyslexic readers Levene Statistic F r2 Non-Words3 47.22 (20.08) 69.94 (11.24) 33.92 (12.85) 7.27*** 43.53*** (.44)1 -.40*** Phoneme Deletion 97% (5%) 96% (6%) 80% (17%) 21.09*** 30.08*** (.37)1 -.39*** Pig Latin 26% (6%) 25% (8%) 18% (11%) 20.75*** 12.06*** (.22)1 -.41*** Spoonerism 24% (7%) 27% (4%) 18% (9%) 5.49** 8.98*** (.23)1 -.35*** 1 For arsine-transformed data 2 Correlation with TOJ threshold 3 Correct words per minute **p<.01; ***p<.001 41 Table 4. Summary of group difference results in all study measures Measure Group differences TOJ (Lower thresholds reflect superior performance) Y< (SD = Elderly) < Dyslexics Speech Perception Tasks (Higher percent reflects superior performance) Speech in Quiet Y = SD = Elderly Speech in Speech Noise Y > SD > Elderly Speech in White Noise (Y = Elderly) > SD 60% Compressed Speech (Y = Elderly) > SD Phonological Awareness Tasks (Higher percent reflects superior performance) 42 Non-Words Y > SD > Dyslexics Phoneme Deletion (Y = SD) > Dyslexics Pig Latin (Y = SD) > Dyslexics Spoonerism (Y = SD) > Dyslexics 43 Figure 1. TOJ thresholds’ means and standard deviations for the study groups 44
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