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Insufficient sleep impairs driving performance and cognitive function
Neuroscience Letters 469 (2010) 229–233
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Insufficient sleep impairs driving performance and cognitive function Seiko Miyata a , Akiko Noda a,∗ , Norio Ozaki b , Yuki Hara a , Makoto Minoshima a , Kunihiro Iwamoto b , Masahiro Takahashi b , Tetsuya Iidaka b , Yasuo Koike a a b
Nagoya University, School of Health Sciences, 1-1-20 Daiko-minami Higashi-ku, Nagoya, Aichi 461-8673, Japan Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
a r t i c l e
i n f o
Article history: Received 23 September 2009 Received in revised form 24 November 2009 Accepted 1 December 2009 Keywords: Near-infrared spectroscopy Cerebral blood flow Sleep deprivation Cognitive function Driving performance
a b s t r a c t Cumulative sleep deprivation may increase the risk of psychiatric disorders, other disorders, and accidents. We examined the effect of insufficient sleep on cognitive function, driving performance, and cerebral blood flow in 19 healthy adults (mean age 29.2 years). All participants were in bed for 8 h (sufficient sleep), and for <4 h (insufficient sleep). The oxyhaemoglobin (oxyHb) level by a word fluency task was measured with a near-infrared spectroscopy recorder on the morning following sufficient and insufficient sleep periods. Wisconsin card sorting test, continuous performance test, N-back test, and driving performance were evaluated on the same days. The peak oxyHb level was significantly lower, in the left and right frontal lobes after insufficient sleep than after sufficient sleep (left: 0.25 ± 0.13 vs. 0.74 ± 0.33 mmol, P < 0.001; right: 0.25 ± 0.09 vs. 0.69 ± 0.44 mmol, P < 0.01). The percentage of correct responses on CPT after insufficient sleep was significantly lower than that after sufficient sleep (96.1 ± 4.5 vs. 86.6 ± 9.8%, P < 0.05). The brake reaction time in a harsh-braking test was significantly longer after insufficient sleep than after sufficient sleep (546.2 ± 23.0 vs. 478.0 ± 51.2 ms, P < 0.05). Whereas there were no significant correlations between decrease in oxyHb and the changes of cognitive function or driving performance between insufficient sleep and sufficient sleep. One night of insufficient sleep affects daytime cognitive function and driving performance and this was accompanied by the changes of cortical oxygenation response. © 2009 Elsevier Ireland Ltd. All rights reserved.
Our contemporary 24-h society has the potential to promote disorders in circadian rhythm and impairment of concentration and memory, resulting in reduced work efficiency and the possible development of depression. Insufficient sleep has significant health implications, as well as an economic impact. The prevalence of insufficient sleep in the general population is reportedly about 25% [23]. Insufficient sleep is typically a chronic condition, commonly associated with sleep/wake variables. A build-up of sleep deprivation increases daytime sleepiness [3]. Given the relationships between excessive daytime sleepiness, traffic and industrial accidents, life-threatening events [4,14], and cognitive and memory problems [2], an understanding of the influence of insufficient sleep on psychiatric function is important for health practitioners. Near-infrared spectroscopy (NIRS) enables the non-invasive measurement of regional cerebral blood flow, in terms of the relative concentration of oxyhaemoglobin (oxyHb), with a high time resolution [30]. NIRS has been applied to the examination of psychiatric patients as well as healthy subjects [12,16,21,22,31]. Bipolar disorder and major depression are characterized by NIRS as hav-
∗ Corresponding author. Tel.: +81 52 719 1537; fax: +81 52 719 1537. E-mail address: [email protected] (A. Noda). 0304-3940/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2009.12.001
ing delayed and reduced frontal lobe activation, respectively [12]. Furthermore, a task-dependent profile of functional abnormalities has been observed in frontal brain metabolism using NIRS in individuals with schizophrenia [21]. Of all the psychiatric disorders associated with insomnia, depression is the most common; 90% of patients with depression complain about sleep quality [28]. As far as we are aware, few previous studies have investigated the relationship between insufficient sleep and decrease in cerebral blood flow detected by NIRS [19]. Accordingly, we have examined the influence of insufficient sleep on cerebral blood flow, cognitive function, and driving performance in healthy adults. Nineteen healthy adults (10 male, 9 female, mean age 29.2 ± 8.1 years) were enrolled in this study. We selected participants who usually sleep between 6 and 8 h nightly by sleep logs [25]. None of the subjects had a history or symptoms of cardiac, vascular, pulmonary, metabolic, or neurological disease, and none had taken medication before the study, or did so during it. The Nagoya University ethics committee approved all procedures associated with the study. We obtained informed consent in writing from each participant after the nature of the procedures had been fully explained. On natural sleep nights, subjects arrived at the sleep laboratory by 10 pm and was in bed for 8 h (from 11 pm to 7 am next
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morning: sufficient sleep), with polysomnographic monitoring. On controlled sleep nights, subjects were allowed to be in bed between 3 am and 7 am, and their total sleep time was limited to <4 h (insufficient sleep). At 7:30 am, NIRS records, cognitive function tests, and driving performance tests were conducted, and the order of tests were arbitrarily assigned. The relative concentrations of oxyHb were measured with a 52-channel NIRS recorder (Hitachi ETG4000; Hitachi Medical, Tokyo, Japan) while the subject performed a word fluency task [24]. The word fluency task consisted of a 60s pre-task baseline, a 60-s word fluency task, and a 60-s post-task baseline. First, subjects were asked to repeat the syllables /a/, /i/, /u/, /e/, /o/, then to generate as many words as they could with the initial syllables /ka/, /sa/, etc. The three initial syllables were changed every 20 s during the 60-s task. To conclude the task, subjects were asked to repeat the syllables /a/, /i/, /u/, /e/, /o/. All participants were randomly allocated into two groups. One group performed the test first with sufficient, and then with insufficient sleep. The other group performed the tests in the opposite order. For an interval of at least one week, subjects slept as their usual sleep schedule and recorded sleep logs, but did not allow the activities affecting sleep quality (ex. napping, staying late). To minimize potential task–practice effects, all participants were instructed and trained in a word fluency task with NIRS measurements, cognitive function tests, and driving performance tests before the study started. Technicians who performed the NIRS measurements, cognitive function test, and driving performance test were blinded to each subject’s sleep status. In this study, oxyHb was measured with 52-channel NIRS machines at two wavelengths of near-infrared light (695 and 830 nm). The absorption of oxyHb was determined and calculated as described previously [15]. The inter-probe distance of the machine was 3 cm, and the measuring points were 2–3 cm beneath the scalp; that is, at the surface of the cerebral cortices [27]. The probes of the NIRS machines were placed on regions of each subject’s hemisphere according to the international 10/20 system used in electroencephalography. The absorption of nearinfrared light was measured with a time resolution of 0.1 s. We measured the peak oxyHb, the time from the start of the task to the peak oxyHb (time to peak), and the time from the peak oxyHb until return to the baseline level (recovery time) (Fig. 1). In addition, we calculated the area under the NIRS wave using trapezium rule. The trapezium rule works by approximating the region under the graph of the function f(x). The values of three channels in the right frontal area (channels 48–50) and three channels in the left frontal area (channels 45–47) were averaged; these represented areas expressing cognitive function and showing haemodynamic changes reported in previous studies [21,28]. The Wisconsin card sorting test (WCST) [10,13], continuous performance test (CPT) [7], and N-back test [5] were chosen to evaluate possible changes in cognitive function. The WCST [10] was used to measure executive functions, for example, abstract reasoning ability or the ability to shift cognitive strategies in response to changing environmental contingencies. A modified computerized version of the WCST [13] was administered, and the test lasted until 48 cards were sorted. In this study, performance was measured by the following indices: category achievement, total errors, the total reaction time taken to choose a category, perseverative errors of Nelson, and difficulty maintaining set. The CPT was used to measure sustained attention or vigilance. We used the continuous performance test, Identical Pairs Version software, as described previously [7]. A series of four-digit stimuli were presented for a period of 50 ms, with an inter-stimulus interval of 950 ms. Each task consisted of 150 trials of which 30 target trials required a response. In this study, performance was
measured by the percentage of correct responses (% corrects), the percentage of incorrect responses (% errors), the mean reaction time of correct hits, and the signal detection index d-prime (d ), a measure of discriminability computed from “hits” and “false alarms”. The N-back test was used to measure working memory. We used working memory task software that requires subjects to update their mental set continually while responding to previously seen stimuli (i.e., numbers). The details of this test have been described previously [5]. The stimulus duration was 0.4 s, the inter-stimulus interval was 1.4 s, and each test comprised 14 trials. The subjects responded to the stimuli by using the numeric keypad of a PC computer. In the present study, a two-back condition was used, and performance was measured as % corrects and the mean reaction time of correct hits. We tested the daily driving skills associated with traffic accidents using a driving simulator. This simulator software was run on a personal computer (Windows XP platform) equipped with a steering wheel, accelerator, and brake pedal system (Sidewinder; Microsoft). Images from the personal computer were projected onto a 1620 mm × 1220 mm screen via an LCD projector (THLB30NT; Panasonic, Osaka, Japan). While watching the driving scenes on the screen, subjects controlled the speed and position of their car by manipulating the steering wheel, accelerator, and brake pedal. The driving simulation was conducted in a dark, soundattenuated room. A gently winding two-lane road with no other traffic continued throughout road-tracking test for a duration of 5 min. Subjects were instructed to drive at a constant speed of 100 km/h and to maintain the vehicle in the centre of the left-hand lane. The lateral position of the vehicle from the right edge of the left lane was recorded every 10 ms. The standard deviation (SD) of the lateral position (in cm), which indicated weaving, was taken as a performance measure. This test was based on a road-tracking test developed previously [17]. Car-following test included a straight two-lane road with no other traffic, except for a single preceding car. The test duration was 5 min. When the preceding car decelerated, its brake lights came on. As the preceding car accelerated (to 60 km/h) or decelerated (to 40 km/h), the subject was required to maintain the distance between the cars as close to 5 m as possible. The car-following distance was recorded every 10 ms and performance was measured as the coefficient of variation (CV) obtained by dividing the standard deviation of the distance between the cars by the mean value [29]. Harsh-braking test included a straight two-lane road with no traffic; however, there were humanoid models on either side of the left lane. The humanoid models randomly ran onto the road as the subject’s car approached. The subject was instructed to maintain a constant speed of 50 km/h and to avoid hitting the humanoid models by braking as quickly as possible. The brake reaction time was used as a measure of cognitive psychomotor performance, including attention efficiency. Each test consisted of seven brake reaction time trials over a 5-min period, and the mean brake reaction time was calculated from these results [11]. Data are presented as means ± SD. Two-way analysis of variance was performed to analyse two-factor interaction between laterality and sleep duration differences for NIRS results. The NIRS results, cognitive function test, and driving performance test were compared between insufficient sleep and sufficient sleep using a paired t-test. Pearson’s correlation test was used to examine the relationship between decreases in NIRS and impairment in the cognitive function test, and decreases in NIRS and impairment in the driving performance test from sufficient sleep to insufficient sleep. All analyses were performed with the SPSS Software 12.0 package (SPSS, Chicago, IL). Probability (P) values of <0.05 were considered statistically significant.
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Fig. 1. Measurement of the oxyhaemoglobin wave. We measured the peak oxyhaemoglobin (oxyHb), the time from the start of the task to the peak oxyHb (time to peak), and the time from the peak oxyHb until return to the baseline level (recovery time), and calculated the area under the NIRS wave using trapezium rule. The trapezium rule works by approximating the region under the graph of the function f(x). Table 1 Near-infrared spectroscopy findings and results of cognitive function tests and driving performance tests. Sufficient sleep NIRS Peak oxyHb (mmol) Left frontal lobe Right frontal lobe
Insufficient sleep
t-Test P value
0.74 ± 0.33 0.69 ± 0.44
0.25 ± 0.13 0.25 ± 0.09
<0.001 <0.01
OxyHb recovery time (ms) Left frontal lobe Right frontal lobe
48.9 ± 18.2 47.3 ± 13.1
29.6 ± 23.0 27.7 ± 17.5
<0.05 <0.05
Time to peak oxyHb (ms) Left frontal lobe Right frontal lobe
51.5 ± 16.0 55.1 ± 14.8
51.1 ± 28.0 46.9 ± 26.7
NS NS
367.5 ± 185.8 331.7 ± 189.3
81.8 ± 52.2 88.3 ± 79.8
<0.001 <0.001
Area under the NIRS wave (mmol-s) Left frontal lobe Right frontal lobe Cognitive function tests Wisconsin card sorting test Category achieved Total errors Total reaction time (s) Perseverative errors of Nelson Difficulty of maintaining set
6.0 8.7 72.5 0.45 0.27
± ± ± ± ±
0.5 1.9 14.9 0.52 0.65
Continuous performance test % corrects Reaction time (ms) % errors Signal detection index d-prime
96.1 623.5 3.4 3.5
± ± ± ±
4.5 117.8 3.4 0.6
N-back testing test (2-back) % corrects Reaction time (ms)
97.6 ± 4.6 414.5 ± 123.8
95.8 ± 7.7 498.1 ± 271.4
NS NS
Driving performance tests Road-tracking test SD of the lateral position
0.58 ± 0.11
0.63 ± 0.06
NS
Car-following test Coefficient of variation
0.57 ± 0.14
0.63 ± 0.13
NS
478.0 ± 51.2
546.2 ± 23.0
Harsh-braking test Brake reaction time (ms)
6.1 9.5 79.0 0.27 0
± ± ± ± ±
0.3 2.0 14.9 0.65 0
NS NS NS NS NS
86.6 641.5 5.8 2.9
± ± ± ±
9.8 127.4 7.0 0.6
<0.05 NS NS NS
<0.05
OxyHb recovery time: time from peak OxyHb to return to baseline level; time to peak oxyHb: time from start of task to peak oxyHb; Area under the NIRS wave: area under the NRS wave was calculated using trapezium rule (Fig. 1); NIRS: near-infrared spectroscopy, SD: standard deviation.
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Fig. 2. The average of oxyhaemoglobin waves on the morning after a night of sufficient (upper) and insufficient (lower) sleep for all subjects. The oxyhaemoglobin (oxyHb) increased during the word fluency task in the frontal lobe (from channel 43 to channel 52) after one night of sufficient sleep. Although oxyHb increased when the task began following a night of insufficient sleep, it decreased immediately. We averaged result channels 48–50 for right and channels 45–47 for left to analyse NIRS findings. The black bar shows the task duration. ch: channel.
The peak oxyHb in the frontal lobe was significantly lower after insufficient sleep than after sufficient sleep (left: 0.25 ± 0.13 vs. 0.74 ± 0.33 mmol, P < 0.001; right: 0.25 ± 0.09 vs. 0.69 ± 0.44 mmol, P < 0.01). The oxyHb recovery time in the frontal lobe was significantly shorter after insufficient sleep than after sufficient sleep (left: 29.6 ± 23.0 vs. 48.9 ± 18.2 ms, P < 0.05; right: 27.7 ± 17.5 vs. 49.1 ± 16.8 ms, P < 0.05). The area under the NIRS wave in the frontal lobe after insufficient sleep was significantly decreased compared with that after sufficient sleep (left: 81.8 ± 52.2 vs. 367.5 ± 185.8 mmol-s, P < 0.001; right: 88.3 ± 79.8 vs. 331.7 ± 189.3 mmol-s, P < 0.001). There was no significant difference in the number of words generated during the word fluency task between sufficient and insufficient sleep states. There was no significant difference in peak oxyHb between the left and right frontal lobes during sufficient or insufficient sleep. Moreover, there were no significant differences on NIRS findings, cognitive function and driving performance between male and female. The time between the start of a task and peak oxyHb did not differ significantly between insufficient sleep and sufficient sleep states (Table 1 and Fig. 2). Whereas the decrease in oxyHb was not significantly correlated with the changes of cognitive function or driving performance between insufficient sleep and sufficient sleep. The percentage of correct responses on continuous performance testing after insufficient sleep was significantly worse than that after sufficient sleep (86.6 ± 9.8 vs. 96.1 ± 4.5%, P < 0.05). There were no significant differences in category achievement, total errors, reaction time, perseverative errors of Nelson, difficulty of maintaining set of WCST, errors, the reaction time, and the signal detection index d of CPT, or in the percentage of correct responses and reaction time in the N-back test between sufficient and insufficient sleep (Table 1). The brake reaction time in the harsh-braking test after insufficient sleep was significantly longer than that after sufficient sleep (546.2 ± 23.0 vs. 478.0 ± 51.2 ms, P < 0.05). However, there were no significant differences in the SD for the road-tracking test and
CV of the car-following test between insufficient and sufficient sleep(Table 1). We have found that the oxyHb level in the frontal lobe was decreased after only one night of insufficient sleep. In cognitive function testing and driving performance testing, the reaction time was prolonged and concentration declined after insufficient sleep, in comparison with sufficient sleep. One night of insufficient sleep involved in the changes of cortical oxygenation responses to brain activation as well as the deterioration of daytime cognitive function and driving performance. NIRS is often used to diagnose psychiatric disorders such as depression and schizophrenia [27]. In depressed patients, an increase in oxyHb during the word fluency task is less than in healthy adults, and in schizophrenic patients, oxyHb shows a sustained moderate increase during the task and begins to decrease immediately after the end of the task [27]. Patients with sleep disorders often have psychiatric disorders [18]. We have demonstrated that the oxyHb level in the frontal lobe was reduced during the task period, and that the oxyHb recovery time after the end of the task was shorter after insufficient sleep. These characteristic NIRS patterns were similar to those seen in patients with depression or schizophrenia [27]. Analysis of cerebral blood flow changes using NIRS might contribute to a better understanding of the relationship between sleep conditions and psychiatric symptoms. The functioning of the prefrontal cortex appears to be particularly susceptible to the effect of sleep loss [8,26]. The rate of cerebral glucose metabolism is decreased predominantly in the prefrontal cortex after one night of sleep deprivation [26]. The blood oxygen level-dependent response is decreased after 35 h of sleep deprivation, and is associated with impaired verbal recall performance [8]. Although our present study used rather short periods of sleep deprivation, the results are consistent with these studies. We did not examine the effect of sleep restriction on oxyHb in peripheral tissue. Further studies should examine whether short periods of sleep restriction induce decrease in peripheral blood flow.
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Falling asleep when driving is an important causative factor of traffic accidents. Increases in sleepiness and performance lapses, as well as poorer driving performance, are all associated with shorter sleep duration [20]. A single night of sleep deprivation decreases frontal lobe metabolic activity, particularly in the anterior cingulate cortex, resulting in decreased performance in immediate error correction [26]. Temporary deactivation of the frontal lobe selectively impairs the ability to stop an initiated action [6]. These studies support our present findings. The results of the word fluency task did not differ significantly, and decrease in oxyHb of frontal lobes on NIRS was not correlated with impairment of cognitive function or driving performance when individuals had sufficient and insufficient sleep in this study. A previous study has shown that experienced individuals are able to conduct a task they are familiar with without focusing on the task, resulting in less of an increase in cerebral blood flow in the frontal lobe during tasks [9]. Thus, individuals who do not sleep adequately might easily generate words without an increase in cerebral blood flow. However, NIRS can detect the changes in cerebral blood flow affected by insufficient sleep. This method might be sensitive to small changes in cerebral blood flow because of insufficient sleep. This study showed that significant impairment on reaction time on driving performance test and sustained attention on CPT, in contrast, no other cognitive function and driving performance measures did not show significant differences. Sleep loss makes it difficult to sustain alertness, attention, reaction time, and psychomotor vigilance [32]. Binks et al. reported that one night sleep deprivation did not impair on established executive tasks such as the word fluency and WCST. It is likely that the magnitude of performance decrements is directly related to the amount of prolonged and sustained attention that a particular cognitive task requires [1]. In conclusion, the oxyHb response in the frontal lobe for the word fluency task, daytime cognitive function, and driving performance were impaired even after one night of insufficient sleep. These results may thus yield unique information about the importance of sleep for industrial productivity, public safety, and human well-being. Acknowledgments This paper is supported by The Academic Frontier Project for Private Universities, Comparative Cognitive Science Institutes. References [1] P.G. Binks, W.F. Eaters, M. Hurry, Short-term total sleep deprivation does not selectively impair higher cortical functioning, Sleep 22 (1999) 328–334. [2] M. Blagrove, C. Alexander, J.A. Horne, The effect of chronic sleep reduction on the performance of cognitive tasks sensitive to sleep deprivation, Appl. Cogn. Pshycol. 9 (1994) 21–40. [3] M.H. Bonnet, D.L. Arand, Clinical effects of sleep fragmentation versus sleep deprivation, Sleep Med. Rev. 7 (2003) 297–310. [4] J.E. Broman, L.G. Lundh, J. Hetta, Insufficient sleep in the general population, Neurophysiol. Clin. 26 (1996) 30–39. [5] J.H. Callicott, A. Bertolino, V.S. Mattay, F.J. Langheim, J. Duyn, R. Coppola, T.E. Goldberg, D.R. Weinberger, Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited, Cereb. Cortex 10 (2000) 1078–1092. [6] C.D. Chambers, M.A. Bellgrove, M.G. Stokes, T.R. Henderson, H. Garavan, I.H. Robertson, A.P. Morris, J.B. Mattingley, Executive “brake failure” following deactivation of human frontal lobe, J. Cogn. Neurosci. 18 (2006) 444–455. [7] B.A. Cornblatt, N.J. Risch, G. Faris, D. Friedman, L. Erlenmeyer-Kimling, The continuous performance test, identical pairs version (CPT-IP): I. New findings about sustained attention in normal families, Psychiatry Res. 26 (1988) 223–238. [8] S.P.A. Drummond, G.G. Brown, J.C. Gillin, J.L. Stricker, E.C. Wong, R.B. Buxton, Altered brain response to verbal learning following sleep deprivation, Nature 403 (2000) 655–657.
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Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Insufficient sleep impairs driving performance and cognitive function Seiko Miyata a , Akiko Noda a,∗ , Norio Ozaki b , Yuki Hara a , Makoto Minoshima a , Kunihiro Iwamoto b , Masahiro Takahashi b , Tetsuya Iidaka b , Yasuo Koike a a b
Nagoya University, School of Health Sciences, 1-1-20 Daiko-minami Higashi-ku, Nagoya, Aichi 461-8673, Japan Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
a r t i c l e
i n f o
Article history: Received 23 September 2009 Received in revised form 24 November 2009 Accepted 1 December 2009 Keywords: Near-infrared spectroscopy Cerebral blood flow Sleep deprivation Cognitive function Driving performance
a b s t r a c t Cumulative sleep deprivation may increase the risk of psychiatric disorders, other disorders, and accidents. We examined the effect of insufficient sleep on cognitive function, driving performance, and cerebral blood flow in 19 healthy adults (mean age 29.2 years). All participants were in bed for 8 h (sufficient sleep), and for <4 h (insufficient sleep). The oxyhaemoglobin (oxyHb) level by a word fluency task was measured with a near-infrared spectroscopy recorder on the morning following sufficient and insufficient sleep periods. Wisconsin card sorting test, continuous performance test, N-back test, and driving performance were evaluated on the same days. The peak oxyHb level was significantly lower, in the left and right frontal lobes after insufficient sleep than after sufficient sleep (left: 0.25 ± 0.13 vs. 0.74 ± 0.33 mmol, P < 0.001; right: 0.25 ± 0.09 vs. 0.69 ± 0.44 mmol, P < 0.01). The percentage of correct responses on CPT after insufficient sleep was significantly lower than that after sufficient sleep (96.1 ± 4.5 vs. 86.6 ± 9.8%, P < 0.05). The brake reaction time in a harsh-braking test was significantly longer after insufficient sleep than after sufficient sleep (546.2 ± 23.0 vs. 478.0 ± 51.2 ms, P < 0.05). Whereas there were no significant correlations between decrease in oxyHb and the changes of cognitive function or driving performance between insufficient sleep and sufficient sleep. One night of insufficient sleep affects daytime cognitive function and driving performance and this was accompanied by the changes of cortical oxygenation response. © 2009 Elsevier Ireland Ltd. All rights reserved.
Our contemporary 24-h society has the potential to promote disorders in circadian rhythm and impairment of concentration and memory, resulting in reduced work efficiency and the possible development of depression. Insufficient sleep has significant health implications, as well as an economic impact. The prevalence of insufficient sleep in the general population is reportedly about 25% [23]. Insufficient sleep is typically a chronic condition, commonly associated with sleep/wake variables. A build-up of sleep deprivation increases daytime sleepiness [3]. Given the relationships between excessive daytime sleepiness, traffic and industrial accidents, life-threatening events [4,14], and cognitive and memory problems [2], an understanding of the influence of insufficient sleep on psychiatric function is important for health practitioners. Near-infrared spectroscopy (NIRS) enables the non-invasive measurement of regional cerebral blood flow, in terms of the relative concentration of oxyhaemoglobin (oxyHb), with a high time resolution [30]. NIRS has been applied to the examination of psychiatric patients as well as healthy subjects [12,16,21,22,31]. Bipolar disorder and major depression are characterized by NIRS as hav-
∗ Corresponding author. Tel.: +81 52 719 1537; fax: +81 52 719 1537. E-mail address: [email protected] (A. Noda). 0304-3940/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2009.12.001
ing delayed and reduced frontal lobe activation, respectively [12]. Furthermore, a task-dependent profile of functional abnormalities has been observed in frontal brain metabolism using NIRS in individuals with schizophrenia [21]. Of all the psychiatric disorders associated with insomnia, depression is the most common; 90% of patients with depression complain about sleep quality [28]. As far as we are aware, few previous studies have investigated the relationship between insufficient sleep and decrease in cerebral blood flow detected by NIRS [19]. Accordingly, we have examined the influence of insufficient sleep on cerebral blood flow, cognitive function, and driving performance in healthy adults. Nineteen healthy adults (10 male, 9 female, mean age 29.2 ± 8.1 years) were enrolled in this study. We selected participants who usually sleep between 6 and 8 h nightly by sleep logs [25]. None of the subjects had a history or symptoms of cardiac, vascular, pulmonary, metabolic, or neurological disease, and none had taken medication before the study, or did so during it. The Nagoya University ethics committee approved all procedures associated with the study. We obtained informed consent in writing from each participant after the nature of the procedures had been fully explained. On natural sleep nights, subjects arrived at the sleep laboratory by 10 pm and was in bed for 8 h (from 11 pm to 7 am next
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morning: sufficient sleep), with polysomnographic monitoring. On controlled sleep nights, subjects were allowed to be in bed between 3 am and 7 am, and their total sleep time was limited to <4 h (insufficient sleep). At 7:30 am, NIRS records, cognitive function tests, and driving performance tests were conducted, and the order of tests were arbitrarily assigned. The relative concentrations of oxyHb were measured with a 52-channel NIRS recorder (Hitachi ETG4000; Hitachi Medical, Tokyo, Japan) while the subject performed a word fluency task [24]. The word fluency task consisted of a 60s pre-task baseline, a 60-s word fluency task, and a 60-s post-task baseline. First, subjects were asked to repeat the syllables /a/, /i/, /u/, /e/, /o/, then to generate as many words as they could with the initial syllables /ka/, /sa/, etc. The three initial syllables were changed every 20 s during the 60-s task. To conclude the task, subjects were asked to repeat the syllables /a/, /i/, /u/, /e/, /o/. All participants were randomly allocated into two groups. One group performed the test first with sufficient, and then with insufficient sleep. The other group performed the tests in the opposite order. For an interval of at least one week, subjects slept as their usual sleep schedule and recorded sleep logs, but did not allow the activities affecting sleep quality (ex. napping, staying late). To minimize potential task–practice effects, all participants were instructed and trained in a word fluency task with NIRS measurements, cognitive function tests, and driving performance tests before the study started. Technicians who performed the NIRS measurements, cognitive function test, and driving performance test were blinded to each subject’s sleep status. In this study, oxyHb was measured with 52-channel NIRS machines at two wavelengths of near-infrared light (695 and 830 nm). The absorption of oxyHb was determined and calculated as described previously [15]. The inter-probe distance of the machine was 3 cm, and the measuring points were 2–3 cm beneath the scalp; that is, at the surface of the cerebral cortices [27]. The probes of the NIRS machines were placed on regions of each subject’s hemisphere according to the international 10/20 system used in electroencephalography. The absorption of nearinfrared light was measured with a time resolution of 0.1 s. We measured the peak oxyHb, the time from the start of the task to the peak oxyHb (time to peak), and the time from the peak oxyHb until return to the baseline level (recovery time) (Fig. 1). In addition, we calculated the area under the NIRS wave using trapezium rule. The trapezium rule works by approximating the region under the graph of the function f(x). The values of three channels in the right frontal area (channels 48–50) and three channels in the left frontal area (channels 45–47) were averaged; these represented areas expressing cognitive function and showing haemodynamic changes reported in previous studies [21,28]. The Wisconsin card sorting test (WCST) [10,13], continuous performance test (CPT) [7], and N-back test [5] were chosen to evaluate possible changes in cognitive function. The WCST [10] was used to measure executive functions, for example, abstract reasoning ability or the ability to shift cognitive strategies in response to changing environmental contingencies. A modified computerized version of the WCST [13] was administered, and the test lasted until 48 cards were sorted. In this study, performance was measured by the following indices: category achievement, total errors, the total reaction time taken to choose a category, perseverative errors of Nelson, and difficulty maintaining set. The CPT was used to measure sustained attention or vigilance. We used the continuous performance test, Identical Pairs Version software, as described previously [7]. A series of four-digit stimuli were presented for a period of 50 ms, with an inter-stimulus interval of 950 ms. Each task consisted of 150 trials of which 30 target trials required a response. In this study, performance was
measured by the percentage of correct responses (% corrects), the percentage of incorrect responses (% errors), the mean reaction time of correct hits, and the signal detection index d-prime (d ), a measure of discriminability computed from “hits” and “false alarms”. The N-back test was used to measure working memory. We used working memory task software that requires subjects to update their mental set continually while responding to previously seen stimuli (i.e., numbers). The details of this test have been described previously [5]. The stimulus duration was 0.4 s, the inter-stimulus interval was 1.4 s, and each test comprised 14 trials. The subjects responded to the stimuli by using the numeric keypad of a PC computer. In the present study, a two-back condition was used, and performance was measured as % corrects and the mean reaction time of correct hits. We tested the daily driving skills associated with traffic accidents using a driving simulator. This simulator software was run on a personal computer (Windows XP platform) equipped with a steering wheel, accelerator, and brake pedal system (Sidewinder; Microsoft). Images from the personal computer were projected onto a 1620 mm × 1220 mm screen via an LCD projector (THLB30NT; Panasonic, Osaka, Japan). While watching the driving scenes on the screen, subjects controlled the speed and position of their car by manipulating the steering wheel, accelerator, and brake pedal. The driving simulation was conducted in a dark, soundattenuated room. A gently winding two-lane road with no other traffic continued throughout road-tracking test for a duration of 5 min. Subjects were instructed to drive at a constant speed of 100 km/h and to maintain the vehicle in the centre of the left-hand lane. The lateral position of the vehicle from the right edge of the left lane was recorded every 10 ms. The standard deviation (SD) of the lateral position (in cm), which indicated weaving, was taken as a performance measure. This test was based on a road-tracking test developed previously [17]. Car-following test included a straight two-lane road with no other traffic, except for a single preceding car. The test duration was 5 min. When the preceding car decelerated, its brake lights came on. As the preceding car accelerated (to 60 km/h) or decelerated (to 40 km/h), the subject was required to maintain the distance between the cars as close to 5 m as possible. The car-following distance was recorded every 10 ms and performance was measured as the coefficient of variation (CV) obtained by dividing the standard deviation of the distance between the cars by the mean value [29]. Harsh-braking test included a straight two-lane road with no traffic; however, there were humanoid models on either side of the left lane. The humanoid models randomly ran onto the road as the subject’s car approached. The subject was instructed to maintain a constant speed of 50 km/h and to avoid hitting the humanoid models by braking as quickly as possible. The brake reaction time was used as a measure of cognitive psychomotor performance, including attention efficiency. Each test consisted of seven brake reaction time trials over a 5-min period, and the mean brake reaction time was calculated from these results [11]. Data are presented as means ± SD. Two-way analysis of variance was performed to analyse two-factor interaction between laterality and sleep duration differences for NIRS results. The NIRS results, cognitive function test, and driving performance test were compared between insufficient sleep and sufficient sleep using a paired t-test. Pearson’s correlation test was used to examine the relationship between decreases in NIRS and impairment in the cognitive function test, and decreases in NIRS and impairment in the driving performance test from sufficient sleep to insufficient sleep. All analyses were performed with the SPSS Software 12.0 package (SPSS, Chicago, IL). Probability (P) values of <0.05 were considered statistically significant.
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Fig. 1. Measurement of the oxyhaemoglobin wave. We measured the peak oxyhaemoglobin (oxyHb), the time from the start of the task to the peak oxyHb (time to peak), and the time from the peak oxyHb until return to the baseline level (recovery time), and calculated the area under the NIRS wave using trapezium rule. The trapezium rule works by approximating the region under the graph of the function f(x). Table 1 Near-infrared spectroscopy findings and results of cognitive function tests and driving performance tests. Sufficient sleep NIRS Peak oxyHb (mmol) Left frontal lobe Right frontal lobe
Insufficient sleep
t-Test P value
0.74 ± 0.33 0.69 ± 0.44
0.25 ± 0.13 0.25 ± 0.09
<0.001 <0.01
OxyHb recovery time (ms) Left frontal lobe Right frontal lobe
48.9 ± 18.2 47.3 ± 13.1
29.6 ± 23.0 27.7 ± 17.5
<0.05 <0.05
Time to peak oxyHb (ms) Left frontal lobe Right frontal lobe
51.5 ± 16.0 55.1 ± 14.8
51.1 ± 28.0 46.9 ± 26.7
NS NS
367.5 ± 185.8 331.7 ± 189.3
81.8 ± 52.2 88.3 ± 79.8
<0.001 <0.001
Area under the NIRS wave (mmol-s) Left frontal lobe Right frontal lobe Cognitive function tests Wisconsin card sorting test Category achieved Total errors Total reaction time (s) Perseverative errors of Nelson Difficulty of maintaining set
6.0 8.7 72.5 0.45 0.27
± ± ± ± ±
0.5 1.9 14.9 0.52 0.65
Continuous performance test % corrects Reaction time (ms) % errors Signal detection index d-prime
96.1 623.5 3.4 3.5
± ± ± ±
4.5 117.8 3.4 0.6
N-back testing test (2-back) % corrects Reaction time (ms)
97.6 ± 4.6 414.5 ± 123.8
95.8 ± 7.7 498.1 ± 271.4
NS NS
Driving performance tests Road-tracking test SD of the lateral position
0.58 ± 0.11
0.63 ± 0.06
NS
Car-following test Coefficient of variation
0.57 ± 0.14
0.63 ± 0.13
NS
478.0 ± 51.2
546.2 ± 23.0
Harsh-braking test Brake reaction time (ms)
6.1 9.5 79.0 0.27 0
± ± ± ± ±
0.3 2.0 14.9 0.65 0
NS NS NS NS NS
86.6 641.5 5.8 2.9
± ± ± ±
9.8 127.4 7.0 0.6
<0.05 NS NS NS
<0.05
OxyHb recovery time: time from peak OxyHb to return to baseline level; time to peak oxyHb: time from start of task to peak oxyHb; Area under the NIRS wave: area under the NRS wave was calculated using trapezium rule (Fig. 1); NIRS: near-infrared spectroscopy, SD: standard deviation.
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Fig. 2. The average of oxyhaemoglobin waves on the morning after a night of sufficient (upper) and insufficient (lower) sleep for all subjects. The oxyhaemoglobin (oxyHb) increased during the word fluency task in the frontal lobe (from channel 43 to channel 52) after one night of sufficient sleep. Although oxyHb increased when the task began following a night of insufficient sleep, it decreased immediately. We averaged result channels 48–50 for right and channels 45–47 for left to analyse NIRS findings. The black bar shows the task duration. ch: channel.
The peak oxyHb in the frontal lobe was significantly lower after insufficient sleep than after sufficient sleep (left: 0.25 ± 0.13 vs. 0.74 ± 0.33 mmol, P < 0.001; right: 0.25 ± 0.09 vs. 0.69 ± 0.44 mmol, P < 0.01). The oxyHb recovery time in the frontal lobe was significantly shorter after insufficient sleep than after sufficient sleep (left: 29.6 ± 23.0 vs. 48.9 ± 18.2 ms, P < 0.05; right: 27.7 ± 17.5 vs. 49.1 ± 16.8 ms, P < 0.05). The area under the NIRS wave in the frontal lobe after insufficient sleep was significantly decreased compared with that after sufficient sleep (left: 81.8 ± 52.2 vs. 367.5 ± 185.8 mmol-s, P < 0.001; right: 88.3 ± 79.8 vs. 331.7 ± 189.3 mmol-s, P < 0.001). There was no significant difference in the number of words generated during the word fluency task between sufficient and insufficient sleep states. There was no significant difference in peak oxyHb between the left and right frontal lobes during sufficient or insufficient sleep. Moreover, there were no significant differences on NIRS findings, cognitive function and driving performance between male and female. The time between the start of a task and peak oxyHb did not differ significantly between insufficient sleep and sufficient sleep states (Table 1 and Fig. 2). Whereas the decrease in oxyHb was not significantly correlated with the changes of cognitive function or driving performance between insufficient sleep and sufficient sleep. The percentage of correct responses on continuous performance testing after insufficient sleep was significantly worse than that after sufficient sleep (86.6 ± 9.8 vs. 96.1 ± 4.5%, P < 0.05). There were no significant differences in category achievement, total errors, reaction time, perseverative errors of Nelson, difficulty of maintaining set of WCST, errors, the reaction time, and the signal detection index d of CPT, or in the percentage of correct responses and reaction time in the N-back test between sufficient and insufficient sleep (Table 1). The brake reaction time in the harsh-braking test after insufficient sleep was significantly longer than that after sufficient sleep (546.2 ± 23.0 vs. 478.0 ± 51.2 ms, P < 0.05). However, there were no significant differences in the SD for the road-tracking test and
CV of the car-following test between insufficient and sufficient sleep(Table 1). We have found that the oxyHb level in the frontal lobe was decreased after only one night of insufficient sleep. In cognitive function testing and driving performance testing, the reaction time was prolonged and concentration declined after insufficient sleep, in comparison with sufficient sleep. One night of insufficient sleep involved in the changes of cortical oxygenation responses to brain activation as well as the deterioration of daytime cognitive function and driving performance. NIRS is often used to diagnose psychiatric disorders such as depression and schizophrenia [27]. In depressed patients, an increase in oxyHb during the word fluency task is less than in healthy adults, and in schizophrenic patients, oxyHb shows a sustained moderate increase during the task and begins to decrease immediately after the end of the task [27]. Patients with sleep disorders often have psychiatric disorders [18]. We have demonstrated that the oxyHb level in the frontal lobe was reduced during the task period, and that the oxyHb recovery time after the end of the task was shorter after insufficient sleep. These characteristic NIRS patterns were similar to those seen in patients with depression or schizophrenia [27]. Analysis of cerebral blood flow changes using NIRS might contribute to a better understanding of the relationship between sleep conditions and psychiatric symptoms. The functioning of the prefrontal cortex appears to be particularly susceptible to the effect of sleep loss [8,26]. The rate of cerebral glucose metabolism is decreased predominantly in the prefrontal cortex after one night of sleep deprivation [26]. The blood oxygen level-dependent response is decreased after 35 h of sleep deprivation, and is associated with impaired verbal recall performance [8]. Although our present study used rather short periods of sleep deprivation, the results are consistent with these studies. We did not examine the effect of sleep restriction on oxyHb in peripheral tissue. Further studies should examine whether short periods of sleep restriction induce decrease in peripheral blood flow.
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Falling asleep when driving is an important causative factor of traffic accidents. Increases in sleepiness and performance lapses, as well as poorer driving performance, are all associated with shorter sleep duration [20]. A single night of sleep deprivation decreases frontal lobe metabolic activity, particularly in the anterior cingulate cortex, resulting in decreased performance in immediate error correction [26]. Temporary deactivation of the frontal lobe selectively impairs the ability to stop an initiated action [6]. These studies support our present findings. The results of the word fluency task did not differ significantly, and decrease in oxyHb of frontal lobes on NIRS was not correlated with impairment of cognitive function or driving performance when individuals had sufficient and insufficient sleep in this study. A previous study has shown that experienced individuals are able to conduct a task they are familiar with without focusing on the task, resulting in less of an increase in cerebral blood flow in the frontal lobe during tasks [9]. Thus, individuals who do not sleep adequately might easily generate words without an increase in cerebral blood flow. However, NIRS can detect the changes in cerebral blood flow affected by insufficient sleep. This method might be sensitive to small changes in cerebral blood flow because of insufficient sleep. This study showed that significant impairment on reaction time on driving performance test and sustained attention on CPT, in contrast, no other cognitive function and driving performance measures did not show significant differences. Sleep loss makes it difficult to sustain alertness, attention, reaction time, and psychomotor vigilance [32]. Binks et al. reported that one night sleep deprivation did not impair on established executive tasks such as the word fluency and WCST. It is likely that the magnitude of performance decrements is directly related to the amount of prolonged and sustained attention that a particular cognitive task requires [1]. In conclusion, the oxyHb response in the frontal lobe for the word fluency task, daytime cognitive function, and driving performance were impaired even after one night of insufficient sleep. These results may thus yield unique information about the importance of sleep for industrial productivity, public safety, and human well-being. Acknowledgments This paper is supported by The Academic Frontier Project for Private Universities, Comparative Cognitive Science Institutes. References [1] P.G. Binks, W.F. Eaters, M. Hurry, Short-term total sleep deprivation does not selectively impair higher cortical functioning, Sleep 22 (1999) 328–334. [2] M. Blagrove, C. Alexander, J.A. Horne, The effect of chronic sleep reduction on the performance of cognitive tasks sensitive to sleep deprivation, Appl. Cogn. Pshycol. 9 (1994) 21–40. [3] M.H. Bonnet, D.L. Arand, Clinical effects of sleep fragmentation versus sleep deprivation, Sleep Med. Rev. 7 (2003) 297–310. [4] J.E. Broman, L.G. Lundh, J. Hetta, Insufficient sleep in the general population, Neurophysiol. Clin. 26 (1996) 30–39. [5] J.H. Callicott, A. Bertolino, V.S. Mattay, F.J. Langheim, J. Duyn, R. Coppola, T.E. Goldberg, D.R. Weinberger, Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited, Cereb. Cortex 10 (2000) 1078–1092. [6] C.D. Chambers, M.A. Bellgrove, M.G. Stokes, T.R. Henderson, H. Garavan, I.H. Robertson, A.P. Morris, J.B. Mattingley, Executive “brake failure” following deactivation of human frontal lobe, J. Cogn. Neurosci. 18 (2006) 444–455. [7] B.A. Cornblatt, N.J. Risch, G. Faris, D. Friedman, L. Erlenmeyer-Kimling, The continuous performance test, identical pairs version (CPT-IP): I. New findings about sustained attention in normal families, Psychiatry Res. 26 (1988) 223–238. [8] S.P.A. Drummond, G.G. Brown, J.C. Gillin, J.L. Stricker, E.C. Wong, R.B. Buxton, Altered brain response to verbal learning following sleep deprivation, Nature 403 (2000) 655–657.
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