Sleep disruption as a correlate to cognitive and adaptive behavior problems in autism spectrum disorders
Highlights
► Quality of sleep, especially sleep duration, was related to problems with day-time cognitive and adaptive functioning in children with Autism Spectrum Disorder. ► Our examination of children with ASD's sleep deprivation (i.e., few hours of sleep per night) negatively impacted their intellectual ability and verbal skills. ► Parental report of their children's sleep in a 24 h period predicted adaptive behavior, such as daily living and social skills and motor dexterity for children. ► Children who experienced more night waking (e.g., screaming) and more sensitivity to sleeping environment disturbances (e.g., noise) were less likely to be successful with daily living skills. ► Breathing related sleep problems and fewer hours of sleep related most often to problems with perceptual tasks.
Introduction
In 1964, 17-year-old Robert Gardner broke the world record for sleep deprivation by staying awake for 264 h without the aid of stimulants (Ross, 1965). This lack of sleep greatly impaired Mr. Gardner's ability to function. Gardner began to have trouble focusing his eyes by the second day of wakefulness. On day three, he experienced mood changes, nausea, and difficulty saying tongue twisters. In addition to his irritability, on the fourth day, Gardner experienced cognitive problems including difficulty concentrating and lapses in memory. Hallucinations and delusions followed, including mistaking a street sign for a person and believing that he was a famous football player being berated by fans. Throughout the rest of his marathon period of wakefulness, Gardner continued to experience these symptoms in addition to fragmented thinking, slurred speech, and blurred vision.
Similarly, sleep disruption has been shown to impair typically developing (TD) children's and adolescents’ day-time functioning. Schreck (2010) reviewed the diagnostic relationships of sleep problems to day-time behavior for children and adolescents finding significant relationships. Research has supported Schreck's (2010) review, indicating that young children who sleep fewer hours per night continually experience more difficulty with perceptual tasks and cognitive ability measures than children who sleep more (Gruber et al., 2010). The impact of sleep deprivation on children's intellectual functioning also has been shown to impair their academic performance (Fredriksen et al., 2004, Wolfson and Carskadon, 1998).
In addition to lack of sleep in general, specific sleep problems have been shown to have negative effects on cognitive functioning and academic performance in TD children and adolescents. For example, TD children diagnosed with or at risk for sleep-disordered breathing have exhibited more difficulty (a) defining vocabulary words (Suratt et al., 2007); (b) sustaining attention (Blunden et al., 2000, Owens et al., 2000, Suratt et al., 2007), (c) planning and problem solving (Karpinski, Scullin, & Montgomery-Downs, 2008), (d) inhibiting behavior (Karpinski et al., 2008), (e) performing in school (Montgomery-Downs et al., 2003, Urschitz et al., 2003), and (f) remembering (Blunden et al., 2000). Like children with sleep disordered breathing, individuals with other sleep problems (e.g., insomnia) also have experienced difficulties with concentration and memory (Fernandez-Mendoza et al., 2009). O’Brien (2009) has asserted that sleep problems (e.g., poor sleep hygiene, sleep restriction, circadian rhythm problems, sleep-disordered breathing, restless legs syndrome, narcolepsy, and insomnia) also have consistently impaired children's attention. With the exception of restless leg syndrome, these sleep problems have also been associated with poor school performance (O’Brien, 2009).
The understanding of the impacts of sleep problems on day-time functioning becomes more vital for children with developmental disabilities (DD), because they tend to have more sleep problems than TD children (Cotton and Richdale, 2006, Goodlin-Jones et al., 2009, Richdale et al., 2000). The increased amount of sleep problems for this population in combination with the deficits associated with DD (e.g., cognitive deficits) may result in an even more significant impact of sleep problems on day-time behavior. For example, Wiggs and Stores (1996) have reported that children with DD who have experienced more bed-time settling problems, night waking, and early morning waking have displayed a greater intensity and number of disruptive day-time behaviors than those without sleep disturbances.
Like children with DD in general, children with Autism Spectrum Disorders (ASD) have consistently been diagnosed with sleep problems (Couturier et al., 2005, Honomichl et al., 2002, Malow et al., 2006a, Polimeni et al., 2005, Richdale and Prior, 1995, Souders et al., 2009). In fact, research has suggested that those with ASD have more sleep problems than TD children and those with other DDs (Allik et al., 2006b, Giannotti et al., 2008, Krakowiak et al., 2008, Miano et al., 2007, Paavonen et al., 2008, Schreck and Mulick, 2000, Souders et al., 2009, Tani et al., 2003). When compared with TD children, these problems have resulted in inefficient sleep, such as night waking or lack of sleep (Allik et al., 2008, Bruni et al., 2007, Couturier et al., 2005, Elia et al., 2000, Giannotti et al., 2008, Goldman et al., 2009, Goldman et al., 2011, Krakowiak et al., 2008, Limoges et al., 2005, Miano et al., 2007, Øyane and Bjorvatn, 2005, Paavonen et al., 2008, Patzold et al., 1998, Schreck and Mulick, 2000, Souders et al., 2009, Wiggs and Stores, 2004).
One category of sleep problems common in children with ASD, insomnia, presents as difficulty initiating or maintaining sleep (see Richdale & Schreck, 2009). Children who have ASD have been known to engage in escape behavior at bedtime in attempts to avoid having to go to sleep (Allik et al., 2006a, Bruni et al., 2007, Giannotti et al., 2008, Goldman et al., in press, Goldman et al., 2009, Paavonen et al., 2008). Even when children go to bed when asked, they often experience difficulty falling asleep (Allik et al., 2006a, Allik et al., 2006b, Allik et al., 2008, Bruni et al., 2007, Giannotti et al., 2008, Goldman et al., 2009, Goldman et al., in press, Honomichl et al., 2002, Hoshino et al., 1984, Limoges et al., 2005, Miano et al., 2007, Paavonen et al., 2008, Patzold et al., 1998, Richdale, 2001, Richdale and Prior, 1995; Segawa, 1985, as cited in Segawa et al., 1992, Souders et al., 2009, Takase et al., 1998, Tani et al., 2003, Wiggs and Stores, 2004, Williams et al., 2004). Remaining asleep also poses a challenge for this population, as most research has suggested that children with ASD often wake up during the night or early in the morning (Allik et al., 2006a, Allik et al., 2006b, Allik et al., 2008, Bruni et al., 2007, Giannotti et al., 2008, Goldman et al., 2009, Goldman et al., in press, Honomichl et al., 2002, Hoshino et al., 1984, Limoges et al., 2005, Miano et al., 2007, Paavonen et al., 2008, Patzold et al., 1998, Richdale, 2001, Richdale and Prior, 1995; Segawa, 1985 as cited in Segawa et al., 1992, Souders et al., 2009, Takase et al., 1998, Tani et al., 2003, Wiggs and Stores, 2004, Williams et al., 2004).
In addition to insomnia, children with ASD may experience circadian rhythm sleep disorders (i.e., delays in falling asleep, waking in a confused state, feeling sleepy during the day, and waking early in the morning). As discussed above, individuals with ASD often have difficulty maintaining and initiating sleep, suggesting problems establishing appropriate sleep-wake cycles. Preliminary research has supported this notion (Giannotti et al., 2008, Segawa et al., 1992). Children in this population have experienced other sleep-quality problems. These sleep-quality problems, such as parasomnias (e.g., confusional arousal, bedwetting, sleep walking, sleep terrors, nightmare disorders), sleep movement disorders (e.g., restless leg, teeth grinding, periodic leg movements, and stereotypic movements), and sleep disordered breathing likely have contributed to night-waking in ASD (Schreck, in preparation, Schreck and Mulick, 2000). These night waking episodes have disrupted sleep for children with ASD more so than children who are TD or have other DDs (Couturier et al., 2005, Goldman et al., 2011, Giannotti et al., 2008, Polimeni et al., 2005, Schreck and Mulick, 2000, Souders et al., 2009).
These types of sleep problems associated with ASD have received considerably more attention from researchers than clarification of their day-time implications. Therefore, knowledge regarding the influence of sleep problems on cognition and adaptive functioning in this population has remained limited. Preliminary research has suggested that a history of decreased sleep duration or poor sleep quality for children with ASD has correlated with nonverbal intelligence deficits (Elia et al., 2000, Gabriels et al., 2005), communication problems (Schreck, Mulick, & Smith, 2004), and academic performance difficulties (Paavonen, Nieminen-von Wendt, Vanhala, Aronen, & von Wendt, 2003). However, not all researchers have discovered a significant relationship between sleep problems and IQ in a sample of children with autism (Mayes & Calhoun, 2009).
Most of the research discussed above has focused on the influence of sleep problems on cognition and academic performance. However, it is also important to examine the impact of these problems on children's ability to function pragmatically in their natural environment (i.e., adaptive behavior). In addition, some of the findings discussed (e.g., impaired academic performance and cognitive ability) may have been at least partially attributable to social and communication problems inherent in ASD. For example, scores on intelligence tests may have been lower than individuals’ true abilities due to their behavior during the test or inability to take the test. Thus, understanding of the relationship of adaptive behavior to sleep problems may help to clarify these relationships. To this date, we have been able to locate only one study that has investigated these effects of sleep problems to adaptive behavior in children with ASD (Krakowiak et al., 2008). Results of this study have remained equivocal with sleep and adaptive behavior associated, but not particularly for young children with ASD.
Although only the previous study has specifically evaluated adaptive behavior, sleep-problems research has suggested links between sleep problems and adaptive behavior skills. For example, a young girl with ASD and sleep apnea showed great improvement in both sleep and social communication after undergoing a surgical procedure designed to correct disordered breathing during sleep (Malow, McGrew, Harvey, Henderson, & Stone, 2006). Additionally, Schreck et al. (2004) found that specific sleep problems predicted increased expression of autism symptoms that would likely affect adaptive behavior. Specifically, night waking and sensitivity to stimuli in the environment was significantly related to communication problems, while shorter sleep duration predicted social interaction problems. In another study, children classified as poor sleepers had greater social interaction problems than good sleepers (Goldman et al., 2011), suggesting a relationship between sleep disruption and adaptive behavior deficits.
Although this research has suggested that sleep problems in autism may be related to these children's cognitive and adaptive performance, significantly more research with this population must be conducted to understand the effects of these sleep problems. In fact, a recent special interest group meeting at the 2011 International Meeting for Autism Research (IMFAR) concluded that while sleep disturbances remain prevalent and significant in ASD, more research must be conducted to determine the impact of sleep disturbance on cognition and daily functioning in this population (Baker, 2011). The purpose of this study was to provide the initial steps toward meeting the IMFAR special interest group recommendations by delineating the relationships between the sleep behavior in children with ASD and subsequent day-time cognitive and adaptive performance.
Section snippets
Participants
Participant data was collected from a database of diagnostic testing for children seen at a pediatric hospital-affiliated disability assessment clinic. Children with a primary diagnosis (by a licensed psychologist) of Autism or PDD-NOS at the clinic were initially identified (N = 455). Participants also had scores in the files for the Behavioral Evaluation of Disorders of Sleep (BEDS; Schreck, 1998, Schreck et al., 2003). After eliminating participants according to this criterion, the participant
Intelligence
Stepwise multiple regression analyses indicated that children's IQ scores across all IQ domains (i.e., verbal, performance, and full scale) were related to their sleep quantity and sleep quality. We analyzed the predictive ability of BEDS factors (i.e., Expressive Sleep Disturbances, Sensitivity to the Environment, Disoriented Awakenings, and Apnea), BEDS total, and number of hours slept (i.e., hours slept per night, hours slept in the last 24 h, hours napped per day) for full scale IQ, verbal
Discussion
By reporting these relationships among specific cognitive skills, adaptive behavior, and sleep factors for children with ASD, this study took the first step toward meeting the recommendations made by the IMFAR special interest group on sleep. In this study, children with ASD who slept fewer hours on average per night were more likely to perform worse overall with respect to intelligence and verbal skills than children who slept longer. This result corroborated Gruber et al.’s (2010)
Acknowledgements
The authors wish to express appreciation for their hospitality to the staff and postdoctoral fellows at The Nationwide Children's Hospital. Without access to their data, cooperation, and inclusion of sleep assessment in psychological evaluations, this study would not have been possible. The authors would also like to thank Eric Butter for his assistance with locating research assistants to enter data. Finally, thank you to Lindsay Knapp and Preeti Kumar for their assistance in preparation and
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