Circadian fluctuations in glucocorticoid level predict perceptual discrimination sensitivity

نویسندگان

چکیده

•Cortisol and auditory perception in N = 68 human adults at 5 times of day•Higher momentary cortisol levels predicted better pitch discrimination•This glucocorticoid effect held under a set statistical control models•Paves way for studies on neuroendocrinological constraints sensation Slow neurobiological rhythms, such as the circadian secretion (GC) hormones, modulate variety body functions. Whether how endocrine fluctuations also exert an influence perceptual abilities is largely uncharted. Here, we show that phasic increases GC availability prove beneficial to discrimination. In age-varying sample healthy participants, characterize covariation saliva with sensitivity discrimination task five time points across sleep-wake cycle. First, were captured well by relative wake-up overall sleep duration. Second, within individuals, higher just prior behavioral testing ability, expressed steepened psychometric curve. This GCs controls. Our results pave more in-depth determinants sensory encoding perception. Most physiological functions humans rhythmicity (Dibner et al., 2010Dibner C. Schibler U. Albrecht The mammalian timing system: organization coordination central peripheral clocks.Annu. Rev. Physiol. 2010; 72: 517-549Crossref PubMed Scopus (1465) Google Scholar). That is, bodily homeostatic oscillate period about 24 hr are vital adapting organism its environment (Spiga 2014Spiga F. Walker J.J. Terry J.R. Lightman S.L. HPA axis-rhythms.Compr. 2014; 4: 1273-1298Crossref (157) These regulated through endogenous clock system suprachiasmatic nucleus (SCN) pacemaker, synchronizing subordinate tissue clocks located throughout While sensory, perceptual, cognitive all have been shown be subject to—much faster—rhythmicity covary brain states sub-second (“neural oscillations”, e.g. Henry Obleser, 2012Henry M.J. Obleser J. Frequency modulation entrains slow neural oscillations optimizes listening behavior.Proc. Natl. Acad. Sci. U S A. 2012; 109: 20095-20100Crossref (223) Scholar) or seconds-to-minutes scale (e.g., Park 2014Park H.D. Correia S. Ducorps Tallon-Baudry Spontaneous responses heartbeats predict visual detection.Nat. Neurosci. 17: 612-618Crossref (150) Scholar; Rebollo 2018Rebollo I. Devauchelle A.D. Beranger B. Stomach-brain synchrony reveals novel, delayed-connectivity resting-state network humans.eLife. 2018; 7: e33321Crossref (51) Scholar), potential role regulation perception, particular, has received much less attention. system, glucocorticoids (GCs) main effector hypothalamic-pituitary-adrenal (HPA) axis, exhibits prominent (Spencer Deak, 2017Spencer R.L. Deak T. A users guide axis research.Physiol. Behav. 2017; 178: 43-65Crossref (136) Cortisol major recognized psychophysiological research primarily stress hormone, reactive physical emotional (Katsu Iguchi, 2016Katsu Y. Iguchi Cortisol. Part III: Lipophilic Hormones Vertebrates, 533– 595 –532.Handbook Hormones. Academic Press, 2016Google More important current investigation, however, blood levels, approximated level lagging it (Kirschbaum Hellhammer, 1989Kirschbaum Hellhammer D.H. Salivary psychobiological research: overview.Neuropsychobiology. 1989; 22: 150-169Crossref (1114) lowest late afternoon up midnight begin rise again during second half night peak early morning (Pruessner 1997Pruessner J.C. Wolf O.T. Buske-Kirschbaum Auer K.V. Jobst Kirschbaum Free after awakening: reliable biological marker assessment adrenocortical activity.Life 1997; 61: 2539-2549Crossref (997) (Figure 1A). It long-standing hypothesis their dynamics linked function. There evidence different phenomena attention executive general (Roberts 1998Roberts A.C. Robbins T.W. Weiskrantz L. Royal Society (Great Britain). Discussion Meeting Prefrontal Cortex : Executive Cognitive Functions. Oxford University 1998Crossref Understanding this association between hormones sensory-cognitive performance implications notorious relation stress-related hearing disorders (Canlon 2013Canlon Theorell Hasson D. Associations problems humans.Hear. Res. 2013; 295: 9-15Crossref (47) can further our understanding variations like might help regulate Generally, do not know strongly, which direction, impacts function due large dynamic range pathways act upon nervous processes (Di 2009Di Maxson M.M. Franco Tasker J.G. Glucocorticoids glutamate GABA synapse-specific retrograde transmission via divergent nongenomic signaling pathways.J. 2009; 29: 393-401Crossref Hall 2015Hall B.S. Moda R.N. Liston Glucocorticoid mechanisms functional connectivity changes neuropsychiatric disorders.Neurobiol. Stress. 2015; 1: 174-183Crossref (40) Lupien Lepage, 2001Lupien S.J. Lepage M. Stress, memory, hippocampus: can’t live it, without it.Behav. Brain 2001; 127: 137-158Crossref (410) 2002Wolf Convit Thorn E. Leon day profiles elderly mild impairment.Psychoneuroendocrinology. 2002; 27: 777-789Crossref Previous mixed: instance, high baseline associated impaired functions, (Echouffo-Tcheugui 2018Echouffo-Tcheugui J.B. Conner S.C. Himali Maillard P. DeCarli C.S. Beiser A.S. Seshadri Circulating structural measures: Framingham Heart Study.Neurology. 91: 1961-1970Crossref (45) but improved dichotic (Al’Absi 2002Al’Absi Hugdahl K. Lovallo W.R. Adrenocortical altered working memory performance.Psychophysiology. 39: 95-99Crossref (65) Dijckmans colleagues (Dijckmans 2017Dijckmans Tortosa-Martínez Caus N. González-Caballero G. Martínez-Pelegrin Manchado-Lopez Clow Does diurnal cycle explain relationship older adults?.Eur. Aging Phys. Activity. 14: 6Crossref (13) reported tasks participants exhibiting larger variation day. An earlier greater magnitude typical awakening response (CAR, 30–45 min post wake-up) predictive relatively function-related (Evans 2011Evans P.D. Fredhoi Loveday Hucklebridge Aitchison Forte old.Int. Psychophysiol. 2011; 79: 371-377Crossref (60) Scholar, Evans 2012Evans related age.Int. 84: 201-204Crossref (46) generally, assumed decrease secretion, either attenuated CAR slowed elimination stress-induced spikes, impairment subjects (Beluche 2010Beluche Carrière Ritchie Ancelin M.L. prospective study community-dwelling people.Psychol. Med. 40: 1039-1049Crossref (68) Stawski 2011Stawski R.S. Almeida D.M. Lachman M.E. Tun P.A. Rosnick C.B. Seeman naturally occurring daily middle adulthood: everything.J. Gerontol. Ser. B Psychol. Soc. 66: 71-81Crossref (44) Importantly, little known what extent directly. Visual fluctuate Stolz 1987Stolz Aschoff Born Circadian evoked (VEP).Electroencephalogr. Clin. Neurophysiol. Suppl. 1987; 279-283PubMed Tassi Pins, 2009Tassi Pins Diurnal humans?.Chronobiol. Int. 35-48Crossref (17) Clinically, part seminal individuals presenting insufficiency (e.g. characteristic Addison disease), Henkin observed systematic pattern lowered thresholds (i.e. detection) paired (Henkin, 1970Henkin R.I. effects corticosteroids ACTH systems.Prog. 1970; 32: 270-294Crossref (88) case audition, generally (Henkin Daly, 1968Henkin Daly Auditory detection normal man patients adrenal cortical insufficiency: steroids.J. Invest. 1968; 47: 1269-1280Crossref (42) Not least, systemic administration synthetic become mainstay treating various disorders, assuming protective inner ear (Trune Canlon, 2012Trune D.R. Canlon Corticosteroid therapy balance disorders.Anat. Rec. (Hoboken). 1928-1943Crossref (61) directly pertaining present study, there along First respect possible involvement given existence molecular cochlea (Meltser 2014Meltser Cederroth C.R. Basinou V. Savelyev Lundkvist G.S. TrkB-mediated protection against noise trauma murine cochlea.Curr. Biol. 24: 658-663Abstract Full Text PDF (62) inferior colliculus (Park 2016Park J.S. Meltser Identification dysregulation exposure.J. 2016; 36: 5509-5519Crossref (27) addition, sensitivity, both specific (for review, see 2017Basinou function.Hear. 347: 47-55Crossref (28) Note direct impact physiologically plausible: first, experimental exposure stimulates leads damages long term (Al-Mana 2008Al-Mana Ceranic Djahanbakhch O. Luxon L.M. review physiology pathophysiology.Neuroscience. 2008; 153: 881-900Crossref (81) receptors ear, especially (Rarey Curtis, 1996Rarey K.E. Curtis Receptors ear.Otolaryngol. Head Neck Surg. 1996; 115: 38-41Crossref (104) brainstem nuclei involved processing (Jennes Langub, 2000Jennes Langub M.C. Endocrine Targets BT - Neuroendocrinology Physiology Medicine. Humana 2000Google Thus, SCN-controlled (Cederroth 2019Cederroth Weger B.D. Tserga Sarlus H. Magnusson A.K. Kadri Gachon cochlear circulating glucocorticoids.Curr. 2019; 2477-2487 e2476Abstract pathway 2007Canlon Johansson Tahera acoustic trauma.Hear. 2007; 226: 61-69Crossref (79) focus discriminating (i.e., detecting presence of) sounds. We used psychophysical method, two-alternative forced-choice (2AFC) task, describe individual lead here (as proxied cortisol) above beyond expected drivers sex chronological age: performing challenging should steeper curve, indicating state elevated and, thus, abilities. As auxiliary hypotheses, (i) Clinard 2010Clinard C.G. Tremblay K.L. Krishnan A.R. alters representation frequency: from frequency-following recordings.Hear. 264: 48-55Crossref (119) (ii) lower design allowed us confounds cross-sectional age differences when studying large, (N 68), investigated individuals) trait individuals). detail, tested cohort young (age range: 19–30 years) middle-aged 50–70 years; Table S5) measurements covering interval approximately 18 (see Figure recorded duration aligned sampling optimally capture post-awakening subsequent drop (Clow 2010Clow Stalder response: than measure function.Neurosci. Biobehav. 35: 97-103Crossref (397) Wilhelm 2007Wilhelm Kudielka B.M. Schlotz W. Wust Is awakening?.Psychoneuroendocrinology. 358-366Crossref (323) task. Task difficulty was titrated based just-noticeable difference (JND). separate linear mixed-effects models test salivary cohort, understand fluctuation turn, represented slope Each model additional, confounders revealed comparison, accounted daytime measurement (expressed modeled using polynomial regressors second, third order) total (conditional R2 .75; S1 full details). Increased (? ?.16, standard error [SE] .04, p .001, log Bayes factor10 (logBF) 3.2) while over best described cubic trend ?.15, SE .07, .025, logBF ?.13). 2A, captures decline evening 2C). considerable improvement fit inclusion session-specific random intercepts attests (likelihood ratio test; ?21 69.5, < 31.9). Overall did differ significantly younger (?21 2.05, .15, ?1.9; 2B). Neither exhibit clear participants' improve fit, 1.0, .31, ?2.4). analysis 3), probed power measured sensitivity. indicated best-fitting model, operationalized function, influenced cortisol, .47; S2 line increased led heightened .13, .004, 1.4). specifically, illustrated 3A (right panel), increase one unit log(nmol/L) curve 10th JND. To interpret examined per individual. On average, changed 2.71 nmol/L (±sd 0.85 nmol/L) course experiment. subject-specific slopes added illustrative purposes (left consistently observable participants. additional including state- within-subjects) trait-level between-subjects) provided support cortisol-driven participant (within-subject cortisol: ? 1.2; between-subject .23, .56, ?2.7; methods S3 expected, significant compared ?.52, .18, .005, 1.3; 3B). precisely, shallower nearly Participant‘s proved predictor females showing ?.36, .049, –.84; S1). Participants' sleepiness (assessed Karolinska Sleepiness Scale; methods) bias (indicated point subjective equality [PSE] function), performance. these predictors tests, > .067, logBFs ?1.2). Lastly, whether would differentially two groups, despite comparable adults. However, respective interaction .91, .34, investigate ran probing bias. found PSE .44, .2, .027, ?.34). .98, ?2.9, S4). One concern aimed target obvious repetition close succession, three hours). Reassuringly, no training time-of-day outcome evident S2). session 1.6, .21, ?2.1) (linear, quadratic, trend) (all .4, ?2.5). considered possibility link could reflect indirect absence any above) rendered scenario unlikely, still formally causal mediation analysis. 3C, comparison estimated (cubic showed comparably small non-significant change (?.042, 95% confidence [CI] [–.13, .04] vs. ?.029, CI[–.13, .07]) accounting (?.013, CI[–.07, .04]). other words, increasing does provide potentially relationship. abilities, if so, degree? out gather decisive data seemingly simple question. mixed between- within-participants multiple samples assessments cycle, indeed ability. first result lending credibility approach cortisol. highly consistent cortisol-level displacement dependent 2A), concert (taking place 2 3) variance degree. Statistically, dissecting person person) versus state-level session) covaried robustness size 3A: one's own steepens 1/10 JND pitch. Essentially, positive steepness series analyses underscores directness putative causality fills gaps knowledge behavior. will discuss mechanisms, limitations, below. imply that, centrally available accompanied objective ability discriminate broadly view activity preparing action (Habib 2001Habib Gold P.W. Chrousos G.P. stress.Endocrinol. Metab. North Am. 30: 695-728Abstract (298) Enhanced certainly into view. What mechanistic bring be? aim briefly cover mechanistically conceivable paths—one relating established dependence receptor tuning GC-related GABAergic signaling. ample now malfunction Hossain 2008Hossain Hajman Charitidi Erhardt Zimmermann Knipper Prenatal dexamethasone impairs behavior

برای دانلود رایگان متن کامل این مقاله و بیش از 32 میلیون مقاله دیگر ابتدا ثبت نام کنید

اگر عضو سایت هستید لطفا وارد حساب کاربری خود شوید

منابع مشابه

Circadian fluctuations in anxiety disorders.

To the Editor: Predictable rhythmic fluctuations, especially circadian, have been observed in a wide variety of physiologicai and psychological functions. Abno~a~ities of circadian patterns have been documented in people with depression, including a tendency for maximal severity of depression in the morning; however, patients with anxiety or mixed depression/anxiety report a tendency for sympto...

متن کامل

Caspian Sea Level Fluctuations

In this paper the main factors that influence the Caspian Sea level rising and the probable and improbable factors are discussed in detail. A cyclical behavior of the level of the Caspian Sea according to local records was proposed. This cyclic fluctuation of the sea level is the long-term behavior of the sea so that the investigation is not restricted to a specific time interval. The statistic...

متن کامل

How ongoing fluctuations in human visual cortex predict perceptual awareness: baseline shift versus decision bias.

Visual perception fluctuates across repeated presentations of the same near-threshold stimulus. These perceptual fluctuations have often been attributed to baseline shifts--i.e., ongoing modulations of neuronal activity in visual areas--driven by top-down attention. Using magnetoencephalography, we directly tested whether ongoing attentional modulations could fully account for the perceptual im...

متن کامل

Circadian rhythms in rheumatology - a glucocorticoid perspective

The hypothalamic-pituitary-adrenal (HPA) axis plays an important role in regulating and controlling immune responses. Dysfunction of the HPA axis has been implicated in the pathogenesis of rheumatoid arthritis (RA) and other rheumatic diseases. The impact of glucocorticoid (GC) therapy on HPA axis function also remains a matter of concern, particularly for longer treatment duration. Knowledge o...

متن کامل

Bilingual Infants Demonstrate Perceptual Flexibility in Phoneme Discrimination but Perceptual Constraint in Face Discrimination

Perceptual narrowing is a highly significant development associated with the first year of life. It conventionally refers to an orientation toward nativeness whereby infant's perceptual sensitivities begin to align with the phonetic properties of their native environment. Nativeness effects, such as perceptual narrowing, have been observed in several domains, most notably, in face discriminatio...

متن کامل

ذخیره در منابع من


  با ذخیره ی این منبع در منابع من، دسترسی به آن را برای استفاده های بعدی آسان تر کنید

ژورنال

عنوان ژورنال: iScience

سال: 2021

ISSN: ['2589-0042']

DOI: https://doi.org/10.1016/j.isci.2021.102345