Cited by 209Circadian rhythm and melatoninSleep and Wakefulness ResearchSleep and Work-Related Fatigue

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Circadian and wakefulness-sleep modulation of cognition in humans

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Wright, Kenneth P., Lowry, Christopher A., LeBourgeois, Monique K.·2012·Frontiers in Molecular Neuroscience

DOI 10.3389/fnmol.2012.00050PMC PMC3328852

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Abstract

Cognitive and affective processes vary over the course of the 24 h day. Time of day dependent changes in human cognition are modulated by an internal circadian timekeeping system with a near-24 h period. The human circadian timekeeping system interacts with sleep-wakefulness regulatory processes to modulate brain arousal, neurocognitive and affective function. Brain arousal is regulated by ascending brain stem, basal forebrain (BF) and hypothalamic arousal systems and inhibition or disruption of these systems reduces brain arousal, impairs cognition, and promotes sleep. The internal circadian timekeeping system modulates cognition and affective function by projections from the master circadian clock, located in the hypothalamic suprachiasmatic nuclei (SCN), to arousal and sleep systems and via clock gene oscillations in brain tissues. Understanding the basic principles of circadian and wakefulness-sleep physiology can help to recognize how the circadian system modulates human cognition and influences learning, memory and emotion. Developmental changes in sleep and circadian processes and circadian misalignment in circadian rhythm sleep disorders have important implications for learning, memory and emotion. Overall, when wakefulness occurs at appropriate internal biological times, circadian clockwork benefits human cognitive and emotion function throughout the lifespan. Yet, when wakefulness occurs at inappropriate biological times because of environmental pressures (e.g., early school start times, long work hours that include work at night, shift work, jet lag) or because of circadian rhythm sleep disorders, the resulting misalignment between circadian and wakefulness-sleep physiology leads to impaired cognitive performance, learning, emotion, and safety.

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Background
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Background
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“have documented circadian modulation of learning and memory in organisms ranging from the sea slug Aplysia [1, 2] to Homo sapiens [3, 4], and in tasks ranging from working memory [5–8] and passive avoidance [9, 10] to hippocampal-dependent visuospatial memory [5, 11–14] and novel object recognition [14–16].”
Background
The effects of a split sleep–wake schedule on neurobehavioural performance and predictions of performance under conditions of forced desynchrony
Kosmadopoulos, A., Sargent, C., Darwent, D., Zhou, X., Dawson, D. E., & Roach, G. D. (2014) · Chronobiology International · doi:10.3109/07420528.2014.957763 · Cited by 32
“The main effects of circadian phase on neurobehavioural performance found here have been well documented (e.g. Matthews et al., 2012a; Wright et al., 2012; Wyatt et al., 1999).”
Background
Cognitive functioning of female nurses during the night shift: The impact of age, clock time, time awake and subjective sleepiness
Zion, N., & Shochat, T. (2018) · Chronobiology International · doi:10.1080/07420528.2018.1497642 · Cited by 32
“Furthermore, superior performance at 07:00 h may demonstrate the beginning of the rising limb in circadian alertness (Wright et al. 2012).”
Background
Inhibition of casein kinase 1δ/εimproves cognitive-affective behavior and reduces amyloid load in the APP-PS1 mouse model of Alzheimer’s disease
Sundaram, S. S., Nagaraj, S., Mahoney, H. L., Portugues, A., Li, W., Millsaps, K., Faulkner, J., Yunus, A., Burns, C. I., Bloom, C., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-50197-x · Cited by 30
Sleep and circadian rhythm characteristics in individuals from the general population during the French COVID‐19 full lockdown
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Daily rewiring of a neural circuit generates a predictive model of environmental light
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Association of Poor Sleep With Depressive and Anxiety Symptoms by HIV Disease Status: Women's Interagency HIV Study
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Dysregulated clock gene expression and abnormal diurnal regulation of hippocampal inhibitory transmission and spatial memory in amyloid precursor protein transgenic mice
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Effects of Circadian Phase Tailored Light Therapy on Sleep, Mood, and Cognition in Alzheimer’s Disease: Preliminary Findings in a Pivotal Study
Cremascoli, R., Sparasci, D., Giusti, G., Cattaldo, S., Prina, E., Roveta, F., Bruno, F., Ghezzi, C., Cerri, S., Picascia, M., et al. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2021.755322 · Cited by 28
Circadian Rhythms in Cognitive Processes: Implications for School Learning
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Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
Reichert, C., Maire, M., Gabel, V., Viola, A., Götz, T., Scheffler, K., Klarhöfer, M., Berthomier, C., Strobel, W. M., Phillips, C. L. M., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-05695-1 · Cited by 26
The Role of Sleep Duration and Sleep Problems During Childhood in the Development of ADHD in Adolescence: Findings From a Population-Based Birth Cohort
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“Moreover, both executive functions and sleep are regulated by prefrontal cortex function and dopaminergic activity (Cassoff et al., 2012; Mahone & Denckla, 2017; Wright et al., 2012; Zee et al., 2013), providing a mechanism linking both traits.”
Background
Examination of Diurnal Variation and Sex Differences in Hippocampal Neurophysiology and Spatial Memory
Goode, L. K., Fusilier, A. R., Remiszewski, N., Reeves, J. M., Abiraman, K., Defenderfer, M. K., Paul, J. R., McMahon, L. L., & Gamble, K. L. (2022) · eNeuro · doi:10.1523/eneuro.0124-22.2022 · Cited by 28
“Cognitive function is also regulated by the circadian system (Wright et al., 2012) and circadian regulation of performance on hippocampus-dependent memory assays has been demonstrated across several species (Snider et al.”
Background
Regulation of Olfactory Associative Memory by the Circadian Clock Output Signal Pigment-Dispersing Factor (PDF)
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“Circadian peaks and troughs in learning and memory have been documented in humans as well as rodent and invertebrate models (Gerstner & Yin, 2010; Wright et al., 2012) such that misalignments between an organism’s cycling internal clock and external conditions (jetlag, social jetlag, and shift work…”
Background
Time-on-task decrement in vigilance is modulated by inter-individual vulnerability to homeostatic sleep pressure manipulation
Maire, M., Reichert, C., Gabel, V., Viola, A., Krebs, J., Strobel, W. M., Landolt, H., Bachmann, V., Cajochen, C., & Schmidt, C. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00059 · Cited by 26
“…Behavioral Neuroscience www.frontiersin.org March 2014 | Volume 8 | Article 59 | 1 BEHAVIORAL NEUROSCIENCE early morning hours, when the circadian pacemaker promotes maximal sleep drive and the homeostatic sleep pressure is rather high (after ca. 21–24 h of prior wakefulness) (Wright et al., 2012).”
Background
Circadian peak dopaminergic activity response at the biological clock pacemaker (suprachiasmatic nucleus) area mediates the metabolic responsiveness to a high‐fat diet
Luo, S., Zhang, Y., Ezrokhi, M., Li, Y., Tsai, T., & Cincotta, A. H. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12563 · Cited by 24
The impact of sleep deprivation on surgeons' performance during night shifts.
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Cultural inheritance is driving a transition in human evolution
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Awareness of sleepiness: Temporal dynamics of subjective and objective sleepiness
Manousakis, J. E., Mann, N., Jeppe, K. J., & Anderson, C. (2021) · Psychophysiology · doi:10.1111/psyp.13839 · Cited by 23
Sleep Apnea Detection Using EEG: A Systematic Review of Datasets, Methods, Challenges, and Future Directions
Fathima, S., & Ahmed, M. (2025) · Annals of Biomedical Engineering · doi:10.1007/s10439-025-03691-5 · Cited by 24
Human fronto-parietal response scattering subserves vigilance at night
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“Spontaneous quiet eyes-open waking EEG and TMS-evoked EEG potentials (TEP) were recorded 8 times during the prolonged wakefulness period to cover the entire near-24 h circadian cycle, with higher session frequency around the circadian wake maintenance (WMZ) and sleep promoting zones (SPZ) (Dijk and Czeisler, 1995) (11…”
FABP7: a glial integrator of sleep, circadian rhythms, plasticity, and metabolic function
Gerstner, J. R., Flores, C. C., Lefton, M., Rogers, B., & Davis, C. J. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1212213 · Cited by 23
“Exactly how circadian and homeostatic processes interact to organize sleep behavior remains unclear and are likely not operating independently (Deboer et al., 2003, 2007; Easton et al., 2004; Laposky et al., 2005; Wright et al., 2012; Deboer, 2018).”
Background
Sleepiness and Cognitive Performance among Younger and Older Adolescents across a 28-Hour Forced Desynchrony Protocol
Wu, L. J., Acebo, C., Seifer, R., & Carskadon, M. A. (2015) · SLEEP · doi:10.5665/sleep.5250 · Cited by 19
Emotional working memory during sustained wakefulness
Tempesta, D., Gennaro, L. D., Presaghi, F., & Ferrara, M. (2014) · Journal of Sleep Research · doi:10.1111/jsr.12170 · Cited by 21
“Cognitive deterioration due to sleep deprivation is modulated by homeostatic sleep pressure and circadian rhythms (Harrison et al., 2007; Wright et al., 2012).”
Background
Increased Orexin Expression Promotes Sleep/Wake Disturbances in the SOD1-G93A Mouse Model of Amyotrophic Lateral Sclerosis
Liu, R., Sheng, Z., Cai, B., Zhang, Y., & Fan, D. (2015) · Chinese Medical Journal · doi:10.4103/0366-6999.149214 · Cited by 19
“The actions of orexins are mediated by two receptors, orexin‐1 (OX1R) and orexin‐2 (OX2R) receptors.[8,9]”
Background
Decreased circadian fluctuation in cognitive behaviors and synaptic plasticity in APP/PS1 transgenic mice
He, Y., Li, Y., Zhou, F., Qi, J., & Wu, M. (2019) · Metabolic Brain Disease · doi:10.1007/s11011-019-00531-z · Cited by 19
Large cognitive fluctuations surrounding sleep in daily living
Huber, R., & Ghosh, A. (2021) · iScience · doi:10.1016/j.isci.2021.102159 · Cited by 19
The effects of doxepin on stress-induced learning, memory impairments, and TNF-α level in the rat hippocampus.
Azadbakht, A. A., Radahmadi, M., Javanmard, S. H., & Reisi, P. (2015) · Europe PMC (PubMed Central) · Cited by 18
Fighting S leep at N ight: B rain C orrelates and V ulnerability to S leep L oss
Maire, M., Reichert, C., Gabel, V., Viola, A., Phillips, C. L. M., Krebs, J., Scheffler, K., Klarhöfer, M., Strobel, W. M., Cajochen, C., et al. (2015) · Annals of Neurology · doi:10.1002/ana.24434 · Cited by 20
“Sleep-loss–related decrements in cognitive performance are most severe during the biological night.(1) They often originate from a misalignment of circadian and sleep-wake regulatory mechanisms, rendering night work particularly challenging for humans.”
Background
Indoor environment and brain health across the life course: A systematic review
Lu, J., Wu, J., & Chen, Y. (2024) · Building and Environment · doi:10.1016/j.buildenv.2024.112156 · Cited by 17
Circadian rhythms in cognitive functioning among patients with schizophrenia: Impact on signal detection in clinical trials of potential pro-cognitive therapies
Hufford, M. R., Davis, V. G., Hilt, D. C., Dgetluck, N., Geffen, Y., Loebel, A. D., Haig, G. M., Santarelli, L., & Keefe, R. S. E. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.07.018 · Cited by 16
“Thiscircadianpacemakeraffects brain arousal through projections from the master circadian clock, located in the hypothalamic suprachiasmatic nuclei, and via clock gene oscillations in a variety of brain tissues (Wright et al., 2012).”
BackgroundInfluential
Unraveling the complexities of circadian and sleep interactions with memory formation through invertebrate research
Michel, M., & Lyons, L. C. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00133 · Cited by 17
“…deprivation or circadian dysfunction, the circadian clock itself modulates memory in humans and results in optimal times for memory and performance as well as trough phases in which significantly decreased performance in cognitive tasks occurs (Wright et al., 2002, 2006, 2012; Goel et al., 2013).”
Background
Variables associated with reductions in insomnia severity among acutely suicidal patients receiving brief cognitive behavioral therapy for suicide prevention
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Interaction Between Circadian Rhythms, Energy Metabolism, and Cognitive Function
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Light/Clock Influences Membrane Potential Dynamics to Regulate Sleep States
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“In humans, chronic disruption in the circadian clock has been linked tomild cognitive impairment and even dementia and Alzheimer’s disease (183, 184).”
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Impact of time of day on radiology image interpretations
Alshabibi, A. S. A., Suleiman, M. E., Tapia, K. A., Heard, R., & Brennan, P. (2020) · Clinical Radiology · doi:10.1016/j.crad.2020.05.004 · Cited by 14
Protein Phosphatase-Dependent Circadian Regulation of Intermediate-Term Associative Memory
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Harnessing the Web for Population-Scale Physiological Sensing: A Case Study of Sleep and PerformancePreprint
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“In summary, the estimates derived from our model closely capture the initial sleep inertia and the increasing homeostatic sleep drive first discovered through laboratory-based studies [4, 42, 48].”
Background
Per2 Expression Regulates the Spatial Working Memory of Mice through DRD1-PKA-CREB Signaling
Kim, M., Custodio, R. J. P., Lee, H. J., Sayson, L. V., Ortiz, D. M., Kim, B.-N., Kim, H. J., & Cheong, J. H. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02845-z · Cited by 14
“Research on circadian misalignment in humans, which occurs due to various reasons, such as early school start, long work hours, and jet lag, revealed that circadian misalignment is a risk factor for cognitive functions [6, 7].”
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Current Concepts in the Diagnosis and Treatment of Sleep Disorders in the Elderly
Gleason, K., & McCall, W. V. (2015) · Current Psychiatry Reports · doi:10.1007/s11920-015-0583-z · Cited by 13

Authors: Wright, K. P., Lowry, C. A., & LeBourgeois, M. K.
Affiliations: University of Colorado Boulder (US)
Corresponding author: Wright, Kenneth P.
ORCID: Wright, Kenneth P.
Lowry, Christopher A.
LeBourgeois, Monique K.
Venue: Frontiers in Molecular Neuroscience
Publisher: Frontiers Media SA
Published: 2012
Volume: 5
Pages: 50-50
ISSN: 1662-5099 (ISSN-L)
DOI: 10.3389/fnmol.2012.00050
PMC: PMC3328852
OpenAlex: W2073957337
Cited by: 209
References: 178
Citations by year: 2026: 11 · 2025: 9 · 2024: 13 · 2023: 12 · 2022: 14 · 2021: 17 · 2020: 19 · 2019: 15 · 2018: 23 · 2017: 13 · 2016: 11 · 2015: 22 · 2014: 14 · 2013: 9 · 2012: 7
FWCI: 7.31
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc
Locations: Frontiers in Molecular Neuroscience (publishedVersion, cc-by-nc)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institutes of Health
National Heart, Lung, and Blood Institute (R01HL085705, R01HL109706)
National Institute of Mental Health (K01MH074643, R01MH086566, R01MH086539)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
Keywords: circadian rhythm, cognitive performance, brain arousal, suprachiasmatic nucleus, clock genes, circadian misalignment, circadian rhythm sleep disorders, learning and memory, emotions, shift work, jet lag

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Circadian and wakefulness-sleep modulation of cognition in humans

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