INTRODUCTION
Sleep is a special physiological state that occurs cyclically in virtually all living
things. Something very similar to sleep has been observed in a rudimentary rest and
activity behavior (wake-sleep cycle) in animals as inferior on the zoological scale
as insects[1 ]. Defining sleep is not a simple task, since some sleep stages show electrophysiological
patterns similar to wakefulness when breathing patterns, eye movements, electroencephalogram
(EEG), and some body movements are observed, which are completely different from other
sleep stages where stillness and slow waves are observed in the EEG.
Although there have been an increasing number of studies on the subject recently,
the probable role of sleep in our organic functioning has yet to be explored in order
to clarify the impacts of this phenomenon on brain function. According to Eugene &
Masiak, the neurobiological processes that occur during sleep are necessary for the
maintenance of physical and cognitive health in - virtually - all species[2 ]. Sleep, the value of which is ignored by most people, also plays a fundamental role
in maintaining higher cognitive functions that is not yet understood by science despite
recent advances. In everyday life, sleep affects mood, memory, attention, sensory
perception, and reasoning, that is, most of the cognitive aspects that connect people
to their environment[3 ]. Sleep disorders can lead to poor quality of performance and sometimes have serious
health consequences.
During the sleep cycle, some stages are responsible for rejuvenating and restoring
the health of the brain. Generally, sleep is interpreted as an unconscious state,
but brain activity continues to operate in its phases, and in a normal/healthy person,
sleep is divided into two main phases: phases with non-rapid eye movements and phases
with rapid eye movements (represented by NREM and REM, respectively). Recent studies
show that the glymphatic system functions like a garbage disposal during NREM sleep,
meticulously removing the byproducts of cellular waste[4 ].
Sleep deprivation affects all parts of the brain separately and independently, and
its effects are recurrent issues in patients with sleeplessness or insomnia. For example,
the temporal lobe is primarily responsible for speech processing, and patients with
insomnia often report slurred speech due to the brain’s inability to process neuronal
signals at their best. In NREM sleep, histamine neurotransmitters are also turned
off, so that their receptors become sensitive again[2 ]. Therefore, studies often find a correlation between anxiety and partial, or total,
sleep deprivation.
The International Classification of Sleep Disorders (ICSD, 3rd edition) lists seven
majors categories, while the four major sleep complaints include excessive daytime
sleepiness, insomnia, abnormal movements or behaviors during sleep, and inability
to fall asleep at the desired time[5 ]. Since a healthy sleep cycle keeps the brain and body healthy, the right conclusion
to draw is that sleep disorders can significantly disrupt basic brain functions.
Attention is a topic that is widely discussed and studied in science and for which
there are many conceptual definitions depending on the theoretical model, including
psychology and neuroscience[6 ].
In the present study, we start from the theoretical concept of neuropsychology that
there are four types of attention: selective attention, sustained attention, divided
attention, and alternate attention. In the context of sleep disorders, attention provides
a comprehensive overview of its effects on cognition and the brain[7 ].
Hennawy, who has discussed the influence of sleep disorders on Alzheimer’s disease
(AD), develops a brief definition for the subtypes of attention used in this paper[7 ]. Selective attention is defined as the ability to focus on a single stimulus while
blocking out all other distractions. Sustained attention, on the other hand, is defined
as the ability to focus on a specific task for a long period of time. Divided attention
is defined as the ability to attend to several tasks simultaneously. Finally, alternating
attention or switching attention is the ability to effortlessly switch attention between
tasks that require different cognitive demands.
The impact that sleep disorders may have on attention, particularly the specific types
of attention that are most affected, and whether there is such a correlation is not
well understood.
Considering the facts mentioned above, and taking into account the importance of studies
investigating the association between sleep and attention for future public health
research and the lack of studies summarizing the literature on this topic, the aim
of this study was to conduct a systematic review that evaluates the relationship between
sleep disorders and attentional performance.
METHODS
The search was conducted between December 2020 and February 2021, following the guidelines
of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA).
This systematic review was conducted in the SciELO, Medline/PubMed, and Cochrane databases
within a 10-year period (2011-2020), using productions in both Portuguese and English.
The following keywords were used in all databases: “attention and sleep” and “attentional
performance and sleep”.
The inclusion criteria for this review were: productions from the past 10 years with
samples of people aged 18 years or older with sleep disorders, cross-sectional or
longitudinal scientific studies that used attentional tests with psychometric evidence
of validity and reliability, and productions in Portuguese and/or English. Case reports,
literature reviews, and systematic reviews were excluded.
A total of 1,682 references were found (1,327 in Cochrane, 321 in PubMED, and 34 in
SciELO). Of these, 284 were duplicates and were therefore excluded. This left 1,398
references for abstract analysis. Sixty-one articles were selected and retrieved,
and after reading the full-text, 15 were finally included ([Table 1 ]).
Table 1
General information about the 15 studies included in this review, according to the
date of publication.
Study
Sample
Sleep disorder
Tests used
Main findings
Main limitations
Bawden et al.[17 ]
17 patients with polysomnographically diagnosed OSA in brief cognitive tests compared
to 20 healthy controls (n=37)
OSA
MMSE, BCSB, DSS, ESS
OSA patients performed significantly worse than controls in the MMSE, in memory items
from the BCSB, and in DS
Small sample
Waggoner et al.[12 ]
27 male and 2 female police officers (n=29)
Sleep deprivation
KSS, PVT, PSQI, ESS, MAPS
Significant lower scores on attention tests and psychomotor vigilance
Small sample, sleep disorder was self-reported
Moraes et al.[19 ]
38 participants divided into the following groups: Narcoleptic group (13 females;
6 males, mean age=37.58); control group (15 Female; 4 Male, mean age=34.42)
Narcolepsy
ESS-BR, VST, TMT
Narcoleptic patients showed higher degrees of EDS, an impaired executive attention
at a temporal level and lower performance in working memory
Small sample
Karimi et al.[16 ]
72 males, 29 female drivers (n=101)
Hypersomnolence, insomnia, restless legs syndrome, OSA
ESS, KSS, FIS, ISI, IRLSS, Polysomnography, ANT, CTT, MWT
High prevalence of sleep disorders correlated with ANT poor results, improvement after
OSA treatment
Few attention and cognitive tasks
Niu et al.[13 ]
62 nurses in a medical center in Taiwan and classified in two groups: fixed-day-shift
group (control group, n=30) and rotating-shift group (experimental group, n=32)
Sleep deprivation
CPSQI, D2
Significant less selective attention, performance speed and accuracy on the attentional
test were poorer in nurses working night shift than in those working day shift
Only woman participated, sleep deprivation was induced
Oliveira et al.[10 ]
Nursing staff in a hospital in Minas Gerais (n=102)
Sleep deprivation
DSS
Subjects in this study with nocturnal shift have impaired results in attention tests,
and self-report less quality of sleep overall. Important to point out that these individuals
also have greater total sleep hours in comparison.
No sleep tests, even self-reported scales. The correlation is uncertain and the sample
is small.
Castronovo et al.[24 ]
17 patients with OSA and 15 controls (n=32)
OSA
MMSE, TMT, Stroop, ESS, PSQI
OSA patients showed impairments in most cognitive areas. After treatment, patients
showed a significant improvement in sleepiness and in all cognitive tests, except
for total time on Stroop test and Trial Making Test B
Small sample
Fortier-Brochu et al.[26 ]
25 adults with primary insomnia and 16 controls (n=25)
Insomnia
Polysomnographic recordings, spectral analysis of the electroencephalogram, ISI, PASAT,
CPT-II
Individuals with insomnia had poorer overall performance compared to participants
of the control group and committed more errors in attention and episodic memory tasks.
Significant cognitive impairments were more frequent with insomnia.
Small Sample
Djonlagic et al.[14 ]
15 healthy controls and 29 patients with obstructive sleep apnea (n=44)
OSA
Polysomnography, PVT
Instant improvement in attention and vigilance based on PVT results
Small sample
Li et al.[11 ]
23 iRBD patients and 23 controls (n=46)
Idiopathic REM sleep behavior disorder (iRBD)
Polysomnography, MMSE, SCW, TMT, DSS
Negative correlation with the Trail Making B test, episodic verbal memory and non-verbal
learning are the most affected domains in iRBD
Small sample
Luz et al.[18 ]
Thirty-nine mild OSA patients and 25 controls were included (n=64)
OSA
Polysomnography, FOSQ, PVT
There was a statistically significant difference between groups when comparing the
“number of lapses” in PVT
Small sample, pilot study
Lancee et al.[20 ]
Participants with insomnia were divided in two groups: training group (n=67, 49 female
and 18 male) and placebo training group (n=70, 51 female and 19 male).
Insomnia
ISI, DT, PSQI
Scores of attentional biases didn’t change at all, the control group showed the same
results as the main group, and the study wasn’t able to tell the difference
Online application of DT could be a central factor in the results, conclusion doesn’t
show if the attention bias can be altered through this method
Zhao et al.[25 ]
28 male and 36 female patients diagnosed with insomnia in Shanghai (n=64)
Insomnia and Sleep Disturbance
PSQI, ANT
Scores of alerting efficiencies increased more, while scores of total reaction time
decreased more in treatment group, insomnia was found to be associated with higher
scores in the executive control variable of the ANT
Small sample
Richards et al.[15 ]
Older adults, aged 55-89 with Mild Cognitive Impairment and Obstructive Sleep Apnea,
divided into two groups: who used CPAP (experimental group, n=29) and those who did
not use CPAP (control group, n=25)
Mild cognitive impairment (MCI), OSA
Polysomnography, SCW, PVT, ESS
There were significant decreases in daytime sleepiness, and improvement in attention
performance in the two measurements performed, from baseline to six months, and from
baseline to one year in the group that adhered to CPAP use compared to the group that
did not use CPAP.
Study structure found the groups may have been different on unidentified variables
that may have affected the study outcomes, like color/race
Alikhani et al.[23 ]
46 males with HIV infection (n=46)
Sleep disturbances self-reported
PSQI, ISI, ESS, D2
Treating sleep disturbances over a period of six to 12 weeks had a positive impact
on aspects of sleep disturbance, symptoms of depression and anxiety, and cognitive
performance
Small sample
OSA: obstructive sleep apnea.
RESULTS
Among the 15 studies included in this review, it was found that the most common reasons
for exclusion at this stage were studies of children and adolescents, mainly with
Attention Deficit Hyperactivity Disorder (ADHD) (343 studies). These studies are not
required to assess the cognitive part of attention because most of them have treated
previously diagnosed ADHD. In this way, the disturbance found in attentional performance
will influence sleep disorder, and not the other way around. Thus, there is a tendency
to study the consequences of ADHD on healthy sleep, but not to do attentional testing.
Another common reason for exclusion was pharmacological studies that investigated
a specific drug, or the effect of a drug on patients with sleep disorders, but attention
tests were not included (359 studies).
Studies selected from all databases for full-text review were subjected to duplication
checking, which resulted in the exclusion of 284 studies. Subsequently, another 348
papers were excluded for not containing relevant data for the present study, such
as, for example, inducing sleep deprivation in healthy patients. After the entire
process of selecting and applying the eligibility criteria, 15 manuscripts were included
in this systematic review. The whole process of selection and application of eligibility
criteria is shown in the flowchart of the PRISMA Statement in [Figure 1 ].
Figure 1 Flowchart of the review process and study selection.
[Table 1 ] provides general information about the 15 studies included in this review, ordered
by date of publication. The samples were from seven different nationalities: 4 Brazilian,
3 American, 3 Chinese, 1 Dutch, 1 Canadian, 1 Iranian, 1 Swedish, and 1 Italian. The
studies were uniformly published between 2011 and 2020, and the 15 publications have
a cross-sectional and/or longitudinal design.
The sleep disorders found were: insomnia (4), obstructive sleep apnea (OSA) (6), sleep
deprivation (SP) (3), idiopathic REM sleep behavior disorder (iRBD) (1), and narcolepsy
(1). Based on the samples, parameters such as the variety of sleep pathologies, the
selection of tests for application, the duration of the intervention, and the sample
size were analyzed.
Of the six studies that analyzed obstructive sleep apnea, only three performed polysomnographic
testing, and, in addition, three others performed the Mini Mental State Examination
(MMSE), a brief 30-item questionnaire used to screen for cognitive impairment. In
three of these studies, Stroop Color Word Tests (SCWT) were also administered to assess
selective attention, ability to maintain focus on an activity, and speed of information
processing. Four articles used the Psychomotor Vigilance Test (PVT), a task that involves
sustained attention and reaction time and measures the speed with which individuals
respond to a visual stimulus. Five of the fifteen articles found used the Pittsburgh
Sleep Quality Inventory (PSQI), which refers to sleep quality in the past month, and
provides an index of severity and nature of disorder. Seven used the Epworth Sleepiness
Scale (ESS), which is a more specific assessment of sleepiness, and ranges from 0
to 24, with excessive sleepiness characterized for scores above 10.
As can be seen from [Table 1 ], the studies do not indicate a strong bias toward the use of any specific test of
attention; they simply show that they test more sustained and selective attention.
It was also not possible to determine a mean or mode of the attention test results,
since it comes from different sleep disorders and this correlation would not be reliable
or strong. However, it should be noted that 40% of the studies used the Pittsburgh
scale to assess sleep quality, and of the six articles that used PSQI, five of them
assessed sustained attention.
DISCUSSION
Sleep disorders are highly heterogeneous in terms of their causative factors, clinical
presentation, and morbidity, making knowledge of the neurological aspects of sleep
and the most common sleep disorders essential for a better understanding of the phenomenon.
The presence of a sleep disorder correlates with decreased alertness and difficulty
in maintaining focus[8 ].
This systematic review, therefore, sought to analyze the relationship between sleep
disturbance and attentional performance and which type of attention is more impacted
or not according to the results of this study. In its most general form, attention
can be described as a general level of alertness or the ability to engage with the
environment. Likewise, this study focused on the types of attention most commonly
described in neuropsychology, namely selective attention, sustained attention, divided
attention, and alternate attention. The selected articles sought to answer how sleep
disorders such as insomnia, obstructive sleep apnea, narcolepsy, and others impact
some of these types of attention.
Among the fifteen studies found, there seems to be a trend toward tests related to
sustained attention. Seven studies examined only sustained attention (46.6%), and
two evaluated only selective attention (13.3%). Five papers evaluated both types of
attention (33.3%), one of the manuscripts analyzed divided attention and selective
attention (6.6%), and none of the papers evaluated alternating attention. A Brazilian
study addressed executive functions and used the term ‘executive attention’ to refer
to a mechanism of attention called Supervised Attentional System (SAS), which deals
with inhibitory control of automatic responses as in the Norman and Shallice’s (1986)
model[9 ]. In the present study, we did not consider this concept of attention because it
is still discussed by most authors as an executive function skill rather than an attentional
skill. It is important to mention that the study of Oliveira et al. (2013) used a
type of attention test that can include divided attention, as it is described as “complex
attention” or attention as an assessable unit ([Table 2 ])[10 ].
Table 2
Information about the type of attention and intervention observed in the included
studies.
Study
Design
Sample (n)
Nation
Attention type
Intervention?
Bawden et al.[17 ]
Experimental/Clinical Trial
37
Brazil
Sustained
Yes
Waggoner et al.[12 ]
Experimental/Randomized Controlled Trial
29
USA
Sustained
No
Moraes et al.[19 ]
Prospective case-control
19
Brazil
Selective
No
Karimi et al.[16 ]
Experimental/Clinical Trial
101
Sweden
Selective, Sustained
Yes
Niu et al.[13 ]
Experimental/Randomized Controlled Trial
62
China
Sustained
Yes
Oliveira et al.[10 ]
Descriptive and observational
102
Brazil
Selective, “Complex Attention”
No
Castronovo et al.[24 ]
Experimental/Clinical Trial
32
Italy
Selective, Sustained
Yes
Fortier-Brochu et al.[26 ]
Prospective case-control
25
Canada
Sustained
No
Djonlagic et al.[14 ]
Experimental/Controlled Clinical Trial
44
USA
Sustained
Yes
Li et al.[11 ]
Prospective case-control
46
China
Selective, Sustained
No
Luz et al.[18 ]
Prospective case-control
64
Brazil
Sustained
No
Lancee et al.[20 ]
Experimental/Randomized Controlled Trial
137
Netherlands
Selective
Yes
Zhao et al.[25 ]
Experimental/Randomized Controlled Trial
64
China
Selective, Sustained
Yes
Richards et al.[15 ]
Experimental/Clinical Trial
25
USA
Selective, Sustained
Yes
Alikhani et al.[23 ]
Experimental/Randomized Controlled Trial
46
Iran
Sustained
Yes
Among the studies that addressed sleep disorders and tested sustained attention, there
was no preference in the tests chosen for evaluation. Of the twelve studies, four
used the Psychomotor Vigilance Test (PVT), three used the Mini Mental State Examination
(MMSE), which is only a cognitive screening test, two used the Attention Network Test
(ANT) and two used the D2 Attention Test. There was also a study by Li et al. (2016)[11 ] that evaluated sustained attention using the Dot-Probe Test (DT) to assess the applicability
of this test in an online context, which may be a trend for future studies as these
tools are needed in times of social isolation and COVID-19.
It is interesting to note that the impact of sleep disorders on sustained attention
is notorious. In the study by Waggoner et al.[12 ], which observed changes in the nighttime habits of police officers, the PVT test
demonstrated twice as many lapses of attention in sleep-deprived individuals compared
to the control group. This study contrasts interestingly with two other studies in
this review, by Niu and Oliveira, which evaluated the caregivers (in China and Brazil,
respectively). The results of the sustained attention tests show an average deficit
of 25% in the mean score of the Stroop Color Word Test (SCWT) and 14.8% in the Digit
Symbol Substitution Test (DSST)[10 ],[11 ],[12 ],[13 ].
Six of the fifteen studies selected in this review addressed OSA and all evaluated
sustained attention, providing categorical results. Four of these studies performed
some type of intervention, such as double-blind placebo-controlled trials and controlled
clinical trials. An interesting contrast is provided by two studies, both conducted
in the United States by Djonlagic and Richards, who evaluated the Continuous Positive
Airway Pressure (CPAP) treatment, one immediately after the first night of intervention
and the second study with follow-ups of 6 months and 1 year after CPAP intervention[14 ],[15 ]. Both studies provided robust results on cognitive assessment after the use of CPAP.
Djonlagic’s study concluded that OSA patients treated with CPAP on the first night
showed immediate improvement in attentional and vigilance performance the next morning
based on PVT results, and OSA patients using CPAP in a long-term treatment showed
improvement in sleep quality[14 ].
A study by Swedish researchers investigated the prevalence of sleep disorders in Public
Transport Operators (PTOs) and evaluated the effects of interventions on hypersomnolence
and neurocognitive function in individuals diagnosed with OSA[16 ]. This study had a satisfactory sample size, performed several examinations (polysomnography,
electrocardiography, ANT, CTT, sleep scales, among others), and produced very promising
and complete results. Patients diagnosed with an occupational injury during the OSA
intervention (59%) were more likely to have an occupational injury than patients without
OSA (37%, p<0.08). This study was also based on an intervention for recent diagnoses
and demonstrated significant improvements in neurocognitive measures of attention
assessed with the Compensatory Tracking Task (CTT)[17 ].
It is also noteworthy that four Brazilian studies are included in this review. Two
of these studies worked with OSA, one with narcolepsy, and one with sleep deprivation[10 ],[18 ],[19 ],[20 ]. Interestingly, none of the Brazilian studies had an intervention, and with the
exception of Oliveira’s study (n=102), the samples were relatively small (average=40).
The study by Moraes was the only one that addressed narcolepsy and assessed attention
tests[20 ]. It is important to mention that this study dealt with executive functions, and
the test chosen to assess “executive attention” was the Victoria Stroop Test (VST),
which may be a way to assess this Executive Function (EF)[20 ]. However, the study found that the narcolepsy patients performed significantly slower
on the tests than the control group and took up to twice as long to perform the VST
and TMT-B.
A Dutch study also stands out because its intervention was very different from other
studies[21 ]. Interestingly, this study evaluated insomnia from a therapeutic perspective, using
a randomized, double-blind, placebo-controlled trial design to examine the efficacy
of attentional bias modification (ABM) training in treating insomnia as an alternative
to Cognitive Behavioral Therapy for Insomnia (CBT-I), which is widely used to treat
this sleep disorder.
The Dot-Probe paradigm is a computer-based fast reaction time task in which two clues
appear simultaneously in different locations on a computer screen to assess selective
attention. The study showed that the ABM approach was not appropriate for treating
patients with insomnia and that there were insufficient differences between the ABM-treated
patients and the control group, even on tests of selective attention. Studies such
as these were rare in this systematic review, once the inclusion criteria were attention
tests and randomized trials, and the results showed that there were few such productions.
It is also interesting to mention that all the studies found in this review show impaired
attention in sleep disorders, leading to negative effects on daily life and work.
In this study, it was not possible to properly identify which type of sleep disorder
has a greater impact on selective and sustained attention because of the few number
of studies.
However, recent studies have shown that total sleep deprivation for only 24 hours
already potentially decreases selective and sustained attention, components of attention,
as well as cognitive inhibition, a component of executive functions[22 ]. Experiments by Norton (1970) with a group of college students indicated that selective
attention was the most impacted in sleep-deprived individuals[23 ].
In this review, some authors concluded that attention and episodic memory were the
most affected aspects. Thus, changes in a more basic physiological phenomenon such
as attention were considered additional factors in the global decline in cognitive
performance[18 ]. In turn, Karimi’s study showed that OSA treatment improved drivers’ ability to
maintain alertness and performance in standardized situations involving monotonous
tasks, as well as their selective attention and episodic memory.
The study by Niu and colleagues showed significant results in groups of nurses who
performed tests of attention, indicating that among the types of attention examined
in this study, selective attention was the most impaired, severely affecting professional
practice and prompting organizations to pay more attention to quality sleep education
in this work setting[13 ]. Although this study does not discuss why sleep affects this type of attention,
the results indicate that the loss of precision in tasks involving complex visual
information may result from a decrease in sensitivity or a change in bias response.
Confirming the relationship between the impact of sleep disorders on attention, Zhao
argues that insomnia triggers a variety of negative emotions, including anxious somatic
arousal, rumination, and worry. These negative emotions, in turn, in addition to insomnia
itself, may directly lead to a crucial decline in attentional control. Negative emotions
was not discussed in the other included manuscripts, which encourages future studies
to investigate the correlation between attentional control and emotional comorbidities
resulting from sleep disorders[24 ],[25 ],[26 ].
Also in Zhao’s study, it was discussed that a potential mechanism for the impairment
of executive attentional control often observed in patients with insomnia could be
insufficient slow-wave sleep (SWS) during nighttime sleep. From the perspective of
neurological functioning, a study published in Nature in 2017[27 ] assessing individuals by examining EEG and local field potentials (LFPs) showed
that sleep deprivation alters the functioning of neurons that generate slow and theta
waves during wakefulness. Thus, attention and memory lapses are observed during the
performance of activities.
In the full reading of the manuscripts, the degree of cognitive impairment (mild,
moderate, or severe) was not discussed. What is known is that sleep disorders affect
cognition, but vary widely in terms of the cognitive aspect, the disturbance, and
the severity of the impact.
Of the seven nationalities examined in the studies, the Brazilian results corroborate
the findings of foreign studies, that is, there is a strong correlation between attentional
variations and sleep disorders.
However, it is necessary to conduct further studies with specific samples to better
inform future research, considering the uniqueness of each type of sleep disorder.
Analysis of the articles selected for this systematic review revealed that there is
a significant relationship between sleep and attention performance. In general, the
sleep disorders evaluated in this study are related to greater impacts on sustained
attention than the other types of attention, but selective attention is also severely
compromised.
Despite the strong influence of poor quality of sleep and its impact on attention,
the number of studies on sleep and its correlation with attentional performance is
small. Nationally, few studies correlated these two topics and undertook interventions
to measure their outcomes. Furthermore, most of these the studies are of small sample
sizes, making generalizations to the entire population difficult.
Considering that sleep can affect behavior, emotions, and physical and cognitive development,
as well as attention levels and other cognitive aspects, it is worth noting that poor
sleep habits that may have started in childhood and adolescence can accompany the
person in adulthood and lead to sleep deprivation, resulting in more complex problems.
These diseases can occur at all stages of development, so further research on the
relationship between sleep and attention is needed for scientific progress.
