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. Auditory processing deficit is
common for sleep deprivation, aging, and dyslexia. However, the extent of the deficit is
different among these groups, and the additional factors affecting their linguistic
performance also might be different, which could explain why although sleep
deprivation, aging and dyslexia all impact TOJ, each one of these groups present different
patterns of linguistic performance.
29
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Table 1. 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