Sleep and executive functions in older adults: A systematic review

A recent increase in studies suggests a role of age-related sleep changes in executive functions (EF). However, this relationship remains unclear and mixed results have emerged.

Objective:

To investigate how age-related sleep changes may play an important role in the extent to which healthy older adults exhibit decline in EF.

Methods:

A systematic strategy was employed to identify the available literature on age-related sleep changes and EF. Results: Of the 465 studies identified, 26 were included.

Results

suggest that multiple sleep parameters differ in the way they benefit or impair EF. Parameters such as greater wake after sleep onset and lower sleep efficiency, in addition to circadian fragmentation of sleep, showed more consistent results and are potentially correlated with worsening in EF measures. However, other results seem inconclusive.

Conclusion:

These findings were discussed based on the prefrontal circuitry vulnerability model, in which sleep has been identified as a beneficial factor for prefrontal cortex functioning and hence for EF, which relies mostly on this brain area and its related networks.

Key words:
executive functions; sleep; older adults; prefrontal cortex

Reference*	Sample	Instruments appplied	Evaluated variables of EF and sleep	Main results	Main limitations
Anderson & Horne⁶⁰60. Anderson C, Horne JA. Prefrontal cortex: links between low frequency delta EEG in sleep and neuropsychological performance in healthy, older people. Psychophysiology. 2003;40:349-357.	N = 24 (10 men and 14 women) Mean age 67 years	EF: WCST, Tower of London, Verbal fluency task, Cattell Test of Fluid Intelligence Sleep: Sleep EEG	EF: Planning, flexibility, verbal fluency, fluid intelligence Sleep: Non REM period	The study found significant associations between 0.5-1.0 Hz power from the left frontal EEG channel, in the first non-REM period, and performance at tasks more specific to the left PFC (e.g., nonverbal planning and verbal fluency).	Age range and number of participants relatively small.
Blackwell et al.³⁸38. Blackwell T, Yaffe K, Ancoli-Israel S, et al. Poor sleep is associated with impaired cognitive function in older women: The study of osteoporotic fractures. J Gerontol A Biol Sci Med Sci 2006;6:405-410.	N = 2932 (women) Mean age 83.5 years	EF: TMT (part B) Sleep: Actigraphy	EF: Cognitive flexibility Sleep: WASO, sleep latency, sleep efficiency, total nap time, TST	Compared with women with sleep efficiency >70%, those with <70% had a higher risk of cognitive impairment. Higher sleep latency was associated with higher risk of cognitive impairment, as was higher WASO. There was no significant relationship for TST.	Findings are for older women and may not be generalizable to other populations such as men.
Schmutte et al.⁵⁰50. Schmutte T, Harris S, Levin R, Zweig R, Katz M, Lipton R. The relation between cognitive functioning and self-reported sleep complaints in nondemented older adults: results from the Bronx aging study. Behav Sleep Med. 2007;5:39-56.	N = 375 (134 men and 241 women) Mean age 79.6 years	EF: Similarities (WAIS III), Digit span (WAIS III), Block design (WAIS III), DSST (WAIS III) Sleep: 54-item sleep questionnaire	EF: Abstract reasoning, working memory, visual-spatial reasoning, processing speed Sleep: Self-reported sleep duration, self-onset latency	Participants who reported longer sleep onset latencies performed significantly worse on measures of verbal knowledge, long-term memory and fund of information, and visuospatial reasoning. Participants who reported longer sleep durations did significantly worse on a measure of verbal short-term (working) memory.	The sleep measure created for the study has no documented psychometric properties. Absence of any objective corroborating data such as PSG.
Yaffe et al.³⁹39. Yaffe K, Blackwell T, Barnes DE, Ancoli-Israel S, Stone KL. Preclinical Cognitive Decline and Subsequent Sleep Disturbance in Older Women. Neurology. 2007;69:237-422.	N = 2474 (women) Mean age 68.9 years	EF: TMT (part B) Sleep: Actigraphy	EF: Cognitive flexibility Sleep: WASO, sleep latency, sleep efficiency, total nap time, TST	Women who declined on Trails B experienced worse sleep efficiency, sleep latency, and wake after sleep onset. Women who declined on Trails B napped more. There was not association with total sleep time.	Actigraphy was performed only at follow-up. Cognitive battery was somewhat limited and only included measures of global cognition and EF.
Gamaldo et al.⁵³53. Gamaldo AA, Allaire JC, Whitfield KE. The Relationship Between Reported Problems Falling Asleep and Cognition Among African American Elderly. Res Aging. 2008;30:752-767.	N = 174 (51 men and 123 women) Mean age 72.7 years	EF: Backward digit span task, Alpha Span task Sleep: Self-reported item asking about trouble falling asleep	EF: Working memory Sleep: Self-reported trouble falling asleep	Self-reported sleep trouble significantly predicted performance on the digit span and alpha span task.	Limited assessment of performance. Self-reported item asking about trouble falling asleep does not account for other possible sleep problems.
Oosterman et al.⁵⁶56. Oosterman JM, Van Someren EJW, Vogels RLC, Van Harten B, Scherder EJA. Fragmentation of the rest-activity rhythm correlates with age-related cognitive deficits. J Sleep Res. 2009;18:129-135.	N = 144 (90 men and 54 women) Mean age 69.5 years	EF: Digit span backward (WAIS III), Stroop test, TMT (part B) Sleep: Actigraphy	EF: Working memory, inhibition, cognitive flexibility Sleep: Sleep fragmentation	The fragmentation of the sleep-wake rhythm predicted all cognitive functions examined. Partial correlations showed that the association of rhythm fragmentation with cognitive decline is partly independent from main effects of age.	Majority of the subjects suffered from at least one cardiovascular risk factor. No objective screening was performed to examine the possible presence of SDB.
Nebes et al.⁴⁸48. Nebes RD, Buysse DJ, Halligan EM, Houck PR, Monk TH. Self-reported sleep quality predicts poor cognitive performance in healthy older adults. J Gerontol B Psychol Sci Soc Sci. 2009;64:180-187.	N = 157 (gender not reported) Mean age 72 years	EF: Perceptual comparison task, N-back, Letter-Number Sequencing (WAIS III), Stroop test, Hayling test, TMT (part B), Test of Nonverbal Intelligence III Sleep: PSQI	EF: Information processing speed, working memory, inhibitory function, attention shifting, abstract reasoning Sleep: Subjective sleep quality, sleep latency, sleep duration, sleep efficiency	Poor sleepers performed significantly worse than good sleepers on measures of general neuropsychological status, abstract reasoning, attention shifting and working memory. It was found that sleep latency and efficiency were correlated with cognitive performance, whereas total sleep duration was not.	Sleep was assessed with a general retrospective self-report measure. There was also no measure of SDB.
Gamaldo et al.⁵²52. Gamaldo AA, Allaire JC, Whitfield KE. Exploring the within-person coupling of sleep and cognition in older African Americans. Psychol Aging. 2010;25:851-857.	N = 50 (11 men and 39 women) Mean age 65.4 years	EF: Stroop test, Clock Drawing Test, Letter Series Test, Letter Fluency. Sleep: PSQI	EF: Inhibition, inductive reasoning, verbal fluency, global executive functioning Sleep: Sleep quality and sleep habits.	A within-person daily change in sleep duration was associated with worse global cognitive performance. The greater an individual deviated away from his/her average sleep duration on a particular day, the more likely his/her performance would decline.	Small sample of only a homogenous group of African American elders. The study relied on subjective rather than objective assessments of sleep.
Blackwell et al.⁴⁰40. Blackwell T, Yaffe K, Ancoli-Israel S, et al. Association of sleep characteristics and cognition in older community-dwelling men: The MrOS sleep study. Sleep. 2011;34:1347-1356.	N = 3132 (men) Mean age 76.4 years	EF: TMT (part B) Sleep: Actigraphy, Sleep diary, PSQI, EES	EF: Mental flexibility Sleep: TST, sleep efficiency, WASO, number of long wake episodes, subjective sleep quality, subjective daytime sleepiness	There were modest cross-sectional associations of wake after sleep onset and self-reported long sleep with cognition among older community dwelling men. Excessive daytime sleepiness and self-reported poor sleep were not related to cognition.	The findings may not be generalizable to populations groups other than community-dwelling older men. Causality cannot be established due to the cross-sectional study design.
Saint Martin et al.⁴⁵45. Saint Martin M, Sforza E, Barthélémy JC, Thomas-Anterion C, Roche E. Does subjective sleep affect cognitive function in healthy elderly subjects? The Proof cohort. Sleep Med. 2012;13:1146-1152.	N = 272 (79 men and 193 women) Mean age 74.8 years	EF: TMT (A and B), Code test (WAIS-III), Similarity test (WAIS-III), Stroop test, Alphabetic Fluency and Category Fluency Tasks, Benton Visual Retention Test (form C) Sleep: PSQI, EES	EF: Attention, shift capacity, rule maintenance capacity, abstractive reasoning, inhibition, verbal fluency, visuospatial working memory Sleep: Subjective sleep quality, excessive daytime sleepiness, sleep duration, sleep latency	Subjective sleep quality and its duration in healthy elderly showed no significant influence on cognitive performance (subjective and objective), except the attention level.	Sleep duration and quality were self-reported and it had no information on sleep structure and sleep fragmentation.
Sagaspe et al.⁵⁹59. Sagaspe P, Taillard J, Amiéva H, et al. Influence of Age, Circadian and Homeostatic Processes on Inhibitory Motor Control: A Go/Nogo Task Study. Plos One. 2012;7(6): e39410.	N = 11 (men) Mean age 68 years	EF: Go/noGo task, Simple Reaction Time Task Sleep: Actigraphy, visual analogue scale sleepiness	EF: Inhibitory motor control, sustained attention Sleep: Sleepiness, sleep deprivation	In the sleep deprivation condition, inhibitory motor control was impaired by extended wakefulness equally in both age groups (young and male). Sustained attention on the executive task decreased under sleep deprivation in both groups, and even more in young participants.	It was not presented.
Sutter et al.⁵¹51. Sutter C, Zöllig J, Allemand M, Martin M. Sleep Quality and Cognitive Function in Healthy Old Age: The Moderating Role of Subclinical Depression. Neuropsychology. 2012;26:768-775.	N = 107 (46 men and 61 women) Mean age 72 years	EF: Regensburg Word Fluency Test, DSST, Subtest 3 of the German Achievement Measure System, Tests of Attentional Performance, TMT (A and B) Sleep: PSQI	EF: Verbal fluency, processing speed, reasoning, inhibition, set-shifting Sleep: Self-reported sleep quality.	Poorer sleep quality was associated with lower performance in reasoning, semantic fluency, and shifting in those with high versus low levels of subclinical depression. Poor sleep quality might affect higher order cognitive processes, particularly in those reporting higher levels of subclinical depression.	Measured each cognitive domain with just one or two single cognitive tests. It did not assess the detailed usage of non-psychoactive medications. The study relied on subjective e assessments of sleep.
Zimmerman et al.⁵⁴54. Zimmerman ME, Bigal ME, Katz MJ, Brickman AM, Lipton RB. Sleep Onset/Maintenance Difficulties and Cognitive Function in Nondemented Older Adults: the Role of Cognitive Reserve. J Int Neuropsychol Soc. 2012;18:461-470.	N = 549 (208 men and 341 women) Mean age 79.7 years	EF: TMT (part B), Category and Letter Fluency test. Sleep: Medical Outcomes Study Sleep Scale	EF: Mental flexibility, set-shifting, concept formation, verbal fluency Sleep: Sleep initiation, sleep maintenance	Older adults with lower education appear selectively vulnerable to the negative effects of sleep onset/maintenance difficulties on tests of verbal fluency.	Determination of sleep onset/maintenance difficulties was based on a self- report questionnaire.
McCrae et al.⁴⁴44. McCrae CS, Vatthauer KE, Dzierzewski JM, Marsiske M. Habitual sleep, reasoning, and processing speed in older adults with sleep complaints. Cogn Ther Res. 2012;36:156-164.	N = 72 (gender not reported) Mean age 70.1 years	EF: Letter Series total Sleep: Sleep diary	EF: Inductive reasoning Sleep: TST, WASO	TST did not predict executive functioning or processing speed. Total wake time did not predict executive functioning but significantly predicted processing speed.	Study's relatively small sample size.
Lim et al.⁵⁷57. Lim AS, Yu L, Costa MD, et al. Increased fragmentation of rest-activity patterns is associated with a characteristic pattern of cognitive impairment in older individuals. Sleep. 2012;35:633-640.	N = 700 (172 men and 528 women) Mean age 82.4 years	EF: Digit span test, Digit ordering test Sleep: Actgraphy	EF: Working memory Sleep: Fragmentation of rest and activity	Greater fragmentation of rest and activity were associated with lower levels of cognitive performance, with preferential involvement of perceptual speed, semantic memory, working memory, and visuospatial abilities.	Primarily women aged 80 and over.
Miyata et al.⁴³43. Miyata S, Noda A, Iwaoto K, Kawano N, Okuda M, Ozaki N. Poor sleep quality impairs cognitive performance in older adults. J Sleep Res. 2013; 22:535-541.	N = 78 (16 men and 62 women) Mean age 72.2	EF: Number (n)-back test Sleep: Actigraphy, PSQI, EES	EF: Working memory Sleep: TST, WASO, sleep efficiency, sleep latency, daytime sleepiness	Short sleep duration decreased short-term memory capacity. Participants with sleep efficiency <85% showed a significant decrease on short-term memory and working memory test accuracy compared with those with sleep efficiency >85%.	The study included a high percentage of female participants.
Wilckens et al.⁴¹41. Wilckens K A, Woo SG, Erickson KI, Wheeler ME. Sleep continuity and total sleep time are associated with task-switching and preparation in young and older adults. J Sleep Res. 2014;23:508-516.	N = 45 (13 men and 32 women) Mean age 62.8 years	EF: Sternberg working-memory task, N-back task, Stroop task, Flanker task, National Adult Reading Test (NART), Categorical and Lexical Fluency tasks Sleep: Sleep detection device	EF: Working memory, inhibition, verbal fluency and proficiency Sleep: WASO, TST	In the older group, higher sleep continuity was associated with better inhibitory control, memory recall, and verbal fluency. TST was not associated with cognitive performance in any domains for the older group.	Participants were not excluded based on any sleep measures or sleep disorders. The study used an accelerometer-based sleep detection device, whereas PSG is considered the "gold standard" for sleep measurement.
Wilckens et al. ⁴²42. Wilckens KA, Woo SG, Kirk AR, Erickson KI, Wheeler ME. The Role of Sleep Continuity and Total Sleep Time in Executive Function Across the Adult Lifespan. Psychol Aging. 2014;29:658-665.	N = 53 (gender not reported) Mean age 62.6	EF: TMT (A and B), DSST (WAIS-III), Stroop Task, N-Back, task-switching Sleep: A sleep detection device	EF: Attention, cognitive flexibility, working memory, inhibition Sleep: WASO, TST	Better global switching performance was associated with longer and more continuous sleep. Young and older adults may benefit similarly from lower wake time after sleep onset and longer total sleep time in overall performance.	The study used an accelerometer-based sleep detection device, whereas PSG is considered the "gold standard" for sleep measurement.
McHugh et al.⁵⁵55. McHugh JE, Walsh L, Lawlor BA. Time to bed is associated with cognitive outcome: an analysis of sleep-times and wake-times in community-dwelling older adults. Biol Rhythm Res. 2014;45:103-114.	N = 505 (gender not reported) Mean age 73.4 years	EF: Digit span backward, CAMCOG similarities, TMT (A and B) Sleep: PSQI	EF: Divided attention, working attention, psychomotor speed Sleep: Time to bed, time do rise	Early and late sleepers were significantly slower on attention, learning and praxis tasks than those whose bedtime did not differ significantly to the robust norm. Wake-times were not associated with cognitive functioning in this cohort.	Self-report measures of sleep. There were no guidelines to categorise morningness-eveningness behavior of a less extreme type among otherwise healthy older adults.
Groeger et al.⁶²62. Groeger JA, Stanley N, Deacon S, Dijk DJ. Dissociating effects of global SWS disruption and healthy aging on waking performance and daytime sleepiness. Sleep. 2014;37:1127-1142.	N= 31 (6 men and 25 women) Mean age 70.8 years	EF: DSST, Sustained attention to Response Task, Choice Reaction Time Test, Lexical Decision Time, Serial Reaction Task, Continuous Tracking Task, Pursuit Tracking Task,Verbal n-Back and Spatial n-Back, Goal Neglect Task, Paced Visual Serial Addition Task, Verbal Fluency Task Sleep: PSG, PSQI	EF: Sustained attention, divided attention, processing speed, decision, sequence & motor control, working memory, verbal fluency. Sleep: Slow wave sleep disruption	Slow wave sleep disruption resulted in less positive affect, slower or impaired information processing and sustained attention, less precise motor control, and erroneous implementation, rather than inhibition, of well-practiced actions. At baseline, younger participants performed better than older participants across many cognitive domains, with largest effects on executive function, response time, sustained attention, and motor control.	It was not presented.
Walsh et al.⁵⁸58. Walsh CM, Blackwell T, Tranah GJ, et al. Weaker circadian activity rhythms are associated with poorer executive function in older women. Sleep 2014;37:2009-2016.	N = 1287 (women) Mean age 82.8 years	EF: Digits Span Backwards (WAIS III); TMT (part B), Categorial and letter fluency Sleep: Actigraphy, PSQI, EES	EF: Working memory, task-switching, attention, verbal production Sleep: Amplitude, mesor, rhythm robustness, acrophase, subjective sleep duration; TST, subjective sleepiness	Weaker circadian activity rhythm patterns were associated with worse cognitive function, especially executive function, in older women without dementia.	Limited to a single sex and primarily Caucasian population. The study did not have detailed cognitive function tests at baseline to control for initial differences in executive function.
Lambiase et al.⁴⁹49. Lambiase MJ, Gabriel KP, Kuller LH, Matthews KA. Sleep and Executive Function in Older Women: The Moderating Effect of Physical Activity. J Gerontol A Biol Sci Med Sci. 2014;69:1170-1176.	N = 121 (women) Mean age 73.3 years	EF: DSST, TMT (A and B), Verbal fluency task Sleep: Actigraphy, Sleep diary	EF: Attention, psychomotor speed, set shifting, mental flexibility, verbal fluency Sleep: TST, sleep efficiency, time to go to bed, time to wake up, sleep latency, number and minutes of awakenings	Sleep efficiency was associated with more correct responses on the DSTT. Sleep was not associated with verbal fluency. Lower sleep efficiency was associated with poorer performance on both the DSST and the TMT B among women with low levels of physical activity but not among women with high levels of physical activity.	The sample was primarily white, well-educated, older women with good overall cognition. The week may not be reflective of habitual sleep or physical activity patterns of the participants.
Lafortune et al.⁶¹61. Lafortune M, Gagnon JF, Martin N, et al. Sleep spindles and rapid eye movement sleep as predictors of next morning cognitive performance in healthy middle-aged and older participants. J Sleep Res. 2014; 23:159-167.	N = 58 (33 men and 25 women) Mean age 63 years	EF: The Bells Test, Conners' Continuous Performance Test II, Verbal fluency task, N-Back task Sleep: PSG	EF: Selective visual attention, inhibition, verbal fluency, working memory Sleep: Spindles, slow wave, sleep latency, REM latency, sleep duration, sleep efficiency, sleep stages (duration)	Spindle density in healthy middle-aged and older participants predicted verbal learning, visual attention and verbal fluency performance. Slow wave density and slow wave slope predicted verbal fluency performance only.	Significant correlations had mild to moderate effect sizes. The first-night effect was not controlled in this study.
Luik et al. ⁴⁷47. Luik AI, Zuurbier LA, Hofman A, Van Someren EJ, Ikram MA, Tiemeier H. Associations of the 24-hour activity rhythm and sleep with cognition: A population-based study of middle-aged and elderly persons. Sleep Med. 2015;16:850-855.	N = 1723 (810 men and 913 women) Mean age 62 years	EF: Letter digit substitution task, Stroop color word test Sleep: Actigraphy, Sleep diary	EF: Sustained attention, psychomotor speed, mental flexibility, inhibition Sleep: Duration actigraphy, interdaily stability, intradaily variability, sleep-onset latency, total sleep time, perceived sleep quality	Persons with less stable 24-h rhythms performed worse on the letter digit substitution task and the stroop interference trial after full adjustment. Similarly, persons with more fragmented rhythms performed worse on the letter digit substitution task and the stroop. Longer observed sleep onset latencies were related to worse performance on the word listening test delayed recall and the categorical word fluency test.	Actigraphy allows to estimate sleep parameters, but it lacks the precision of PSG. The study did not formally assess chronotype. Self-rated but no objective information about sleep-disordered breathing.
Seelye et al.⁴⁶46. Seelye A, Mattek N, Howieson D, Riley T, Wild K, Kaye J. The Impact of Sleep on Neuropsychological Performance in Cognitively Intact Older Adults Using a Novel In-Home Sensor-Based Sleep Assessment Approach. Clin Neuropsychol. 2015;29:53-66.	N = 63 (11 men and 52 women) Mean age 87 years	EF: Letter-Number Sequencing (WMS III), Digit span (forward and backward) (WAIS R), DSST (WAIS R), TMT (Part A and B), Letter fluency, Stroop test Sleep: Sensor-based sleep assessment	EF: Working memory, attention, cognitive flexibility, verbal fluency, inhibition Sleep: Total movement in bed at night, restlessness, times up at night, TST	Mildly disturbed sleep the week prior and month prior to cognitive testing was associated with reduced working memory on cognitive evaluation. One night of mild sleep disturbance was not associated with decreased cognitive performance the next day. Sleep duration was unrelated to cognition.	The number of individuals with diagnosed sleep disorders was unknown.
Song et al.⁶³63. Song Y, Blackwell T, Yaffe K, Ancoli-Israel S, Redline S, Stone KL; Osteoporotic Fractures in Men (MrOS) Study Group. Relationships between sleep stages and changes in cognitive function in older men: the MrOS Sleep Study. Sleep. 2015;38:411-421.	N = 2601 (men) Mean age 76 years	EF: TMT (Part B) Sleep: PSG	EF: Cognitive flexibility Sleep: Sleep stages	Increased time in Stage N1 sleep and less time in Stage REM sleep are associated with worsening cognitive performance in older men over time.	Participants had relatively high levels of cognitive function at baseline (sleep visit) and follow-up. First-night effect caused possibly by single overnight PSG.

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[1] Francisco Wilson Nogueira Holanda Júnior. Postgraduate Program in Psychology / Federal University of Rio Grande do Norte / Lagoa Nova - 59078-970 Mailbox 1622 - Natal RN - Brazil. E-mail: franciscowilson3@hotmail.com