Twitches emerge postnatally during quiet sleep in human infants and are synchronized with sleep spindles

SummaryIn humans and other mammals, the stillness of sleep is punctuated by bursts of rapid eye movements (REMs) and myoclonic twitches of the limbs [1]. Contrary to the notion that twitches are mere by-products of dreams, sensory feedback arising from twitching limbs provides a rich and unique source of activation to the developing sensorimotor system [2]. In fact, it is partly because of the behavioral activation of REM sleep that this state is also called active sleep (AS), in contrast with the behavioral quiescence that gives quiet sleep (QS)—the second major stage of sleep—its name. In human infants, for which AS occupies eight or more hours of each day [3], limb twitching is one among several components that help to identify the state [4-7]; nonetheless, we know relatively little about the structure and functions of twitching across development. Recently, in sleeping infants over the first seven postnatal months [8], we documented a pronounced shift in the temporal expression of twitching beginning around three months of age that suggested a qualitative shift in how twitches are produced. Here, we combine behavioral assessments of twitching with high-density electroencephalography (EEG) and demonstrate that this shift reflects the developmental emergence of limb twitches during QS. Twitches during QS are not only unaccompanied by REMs, but they also occur synchronously with sleep spindles, a hallmark of QS. As QS-related twitching increases with age, sleep spindle rate also increases along the sensorimotor strip. The emerging synchrony between subcortically generated twitches and cortical oscillations suggests the development of functional connectivity among distant sensorimotor structures, with potential implications for detecting and explaining atypical developmental trajectories.

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Development of autonomic heart rate control in the kitten during sleep

AJP Heart and Circulatory Physiology ◽

10.1152/ajpheart.1980.238.6.h829 ◽

1980 ◽

Vol 238 (6) ◽

pp. H829-H835

Author(s):

J. R. Egbert ◽

P. G. Katona

Keyword(s):

Heart Rate ◽

Rate Control ◽

Intrinsic Rate ◽

Blocking Agent ◽

Heart Rate Change ◽

Heart Rate Control ◽

Active Sleep ◽

Quiet Sleep ◽

Human Infants ◽

Sympathetic Control

Development of cardiac rate control was studied in 34 kittens aged 4 days to 6 wk during quiet and active sleep, using atropine and propranolol to quantitatively assess the degree of tonic parasympathetic and sympathetic control, with the analysis based on the Rosenblueth and Simeone model. The order of blocking agent administration did not significantly affect the results if a correction was made for the baroreceptor-mediated heart rate change after the blockade of a single autonomic branch. During the first 4 wk, the heart rate in quiet sleep was lower than in active sleep due to a significantly higher parasympathetic tone. The heart rate decreased with age in both sleep states: the decrease in quiet sleep was accompanied by a transition from sympathetic to parasympathetic dominance. The intrinsic rate of the pharmacologically denervated heart was maximum at about 2 wk and decreased steadily thereafter. The observed changes may help explain some features of the development in heart rate previously reported for sleeping human infants.

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The Case of the Disappearing Spindle Burst

Neural Plasticity ◽

10.1155/2016/8037321 ◽

2016 ◽

Vol 2016 ◽

pp. 1-7 ◽

Cited By ~ 8

Author(s):

Alexandre Tiriac ◽

Mark S. Blumberg

Keyword(s):

Sensorimotor Cortex ◽

Sleep Spindles ◽

Active Sleep ◽

Quiet Sleep ◽

Retinal Waves ◽

Cortical Oscillations ◽

Sensory Activity ◽

Transient Feature ◽

Sensorimotor Systems ◽

Peripheral Sensory

Sleep spindles are brief cortical oscillations at 10–15 Hz that occur predominantly during non-REM (quiet) sleep in adult mammals and are thought to contribute to learning and memory. Spindle bursts are phenomenologically similar to sleep spindles, but they occur predominantly in early infancy and are triggered by peripheral sensory activity (e.g., by retinal waves); accordingly, spindle bursts are thought to organize neural networks in the developing brain and establish functional links with the sensory periphery. Whereas the spontaneous retinal waves that trigger spindle bursts in visual cortex are a transient feature of early development, the myoclonic twitches that drive spindle bursts in sensorimotor cortex persist into adulthood. Moreover, twitches—and their associated spindle bursts—occur exclusively during REM (active) sleep. Curiously, despite the persistence of twitching into adulthood, twitch-related spindle bursts have not been reported in adult sensorimotor cortex. This raises the question of whether such spindle burst activity does not occur in adulthood or, alternatively, occurs but has yet to be discovered. If twitch-related spindle bursts do occur in adults, they could contribute to the calibration, maintenance, and repair of sensorimotor systems.

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Transient changes in expiratory time during hypercapnia in premature infants

Journal of Applied Physiology ◽

10.1152/jappl.1987.62.3.1010 ◽

1987 ◽

Vol 62 (3) ◽

pp. 1010-1013 ◽

Cited By ~ 20

Author(s):

L. M. Noble ◽

W. A. Carlo ◽

M. J. Miller ◽

J. M. DiFiore ◽

R. J. Martin

Keyword(s):

Steady State ◽

Preterm Infants ◽

Premature Infants ◽

Lung Volume ◽

Minute Ventilation ◽

Inspiratory Time ◽

Quiet Sleep ◽

Human Infants ◽

Expiratory Time ◽

Ventilatory Responses

The transient ventilatory responses to hypercapnia were studied in nine healthy preterm infants. We administered 4% CO2 in air for at least 7 min during quiet sleep and measured frequency (f), inspiratory time (TI), expiratory time (TE), tidal volume (VT), and minute ventilation (VI). Frequency increased over the first 2 min of CO2 inhalation (P less than 0.05) and then decreased to control values (P less than 0.05). This response was secondary to changes in TE, which decreased over the first 2 min (P less than 0.05) and then returned to control values, whereas TI did not change. The late increase in TE was associated with an increased percent of breaths exhibiting retardation of expiratory flow (braking) (P less than 0.05). These breaths had longer TE than the breaths without braking (P less than 0.05). Exponential curves made to fit the increases in VI and VT revealed that only 67% of the infants reached 90% of steady state for both VI and VT over the 7-min study period. The time to 90% of steady state was always shorter for VI than VT (P less than 0.05) due to the transient changes in f. The results indicate that the transient changes of f in response to hypercapnia are secondary to changes in TE, which appear unique to human infants. We speculate that the expiratory braking that develops during the course of CO2 inhalation increases lung volume, resulting in prolongation of TE via mechanoreceptor-mediated reflexes.

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A quantitative method for classification of EEG in the fetal baboon

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1993.265.3.r706 ◽

1993 ◽

Vol 265 (3) ◽

pp. R706-R714

Author(s):

M. M. Myers ◽

R. I. Stark ◽

W. P. Fifer ◽

P. G. Grieve ◽

J. Haiken ◽

...

Keyword(s):

Spectral Power ◽

Quiet Sleep ◽

Human Infants ◽

Eeg Activity ◽

Spectral Edge Frequency ◽

Visual Coding ◽

Ovine Fetus ◽

Composite Parameter ◽

The Individual

Electroencephalographic (EEG) activity is used as a primary indicator of sleep states in adults and infants of many species and in the ovine fetus. We recently reported that the baboon fetus exhibits visually discernable patterns of EEG activity. One pattern of activity, characterized by the intermittent presence of repetitive bursts of high-voltage EEG, is indistinguishable from trace alternant (TA). TA is a distinctive pattern of EEG activity found only during early stages of development in primates. TA is the predominant pattern of EEG activity during quiet sleep in human infants < 2 mo of age. The focus of this study was to derive quantitative parameters that would discriminate TA from other activity and then to develop a method for automated categorization of EEG patterns. Results demonstrate that several parameters derived from frequency-domain analyses are related to visually coded EEG states. Among these parameters, high-frequency power (12-24 Hz) and spectral-edge frequency are good discriminators of EEG patterns. This paper describes a new parameter, EEG ratio, computed as spectral power in the rectified EEG within a band that corresponds to the frequency of bursts of activity during TA (0.03-0.20 Hz) divided by power in the 12- to 24-Hz band. This new composite parameter of EEG activity provides a markedly better correlate of visually coded EEG than any of the individual parameters tested. Using cluster analysis, we devised a method for objective minute-by-minute dichotomization of EEG ratio. The method produces results that agree with visual coding of EEG activity 87.1% of the time.(ABSTRACT TRUNCATED AT 250 WORDS)

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Influence of sleep state on frequency of swallowing, apnea, and arousal in human infants

Journal of Applied Physiology ◽

10.1152/japplphysiol.00361.2002 ◽

2003 ◽

Vol 94 (6) ◽

pp. 2456-2464 ◽

Cited By ~ 17

Author(s):

Garrick W. Don ◽

Karen A. Waters

Keyword(s):

Sleep Stage ◽

Respiratory Rhythm ◽

Active Sleep ◽

Sleep State ◽

Quiet Sleep ◽

Human Infants ◽

The Mean ◽

Swallowing Apnea

Apnea and arousal are modulated with sleep stage, and swallowing may interfere with respiratory rhythm in infants. We hypothesized that swallowing itself would display interaction with sleep state. Concurrent polysomnography and measurement of swallowing allowed time-matched analysis of 3,092 swallows, 482 apneas, and 771 arousals in 17 infants aged 1–34 wk. The mean rates of swallowing, apnea, and arousal were significantly different, being 23.3 ± 8.5, 9.4 ± 8.8, and 15.5 ± 10.6 h−1, respectively ( P < 0.001 ANOVA). Swallows occurred before 25.2 ± 7.9% and during 74.8 ± 6.3% of apneas and before 39.8 ± 6.0% and during 60.2 ± 6.0% of arousals. The frequencies of apneas and arousals were both strongly influenced by sleep state (active sleep > indeterminate > quiet sleep, P < 0.001), whether or not the events coincided with swallowing, but swallowing rate showed minimal independent interaction with sleep state. Interactions between swallowing and sleep state were predominantly influenced by the coincidence of swallowing with apnea or arousal.

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Cross-species invariance in state-related motility patterns

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1981.241.5.r312 ◽

1981 ◽

Vol 241 (5) ◽

pp. R312-R315

Author(s):

E. B. Thoman ◽

L. P. Zeidner ◽

V. H. Denenberg

Keyword(s):

Direct Observation ◽

Single Channel ◽

Temporal Distribution ◽

Critical Parameters ◽

Quiet Sleep ◽

Human Infants ◽

Extensive Experience ◽

Analog Signals ◽

Exact Agreement ◽

Analog Movement

Each of the sleep and wake states of animals are characterized by specific patterns of behavioral, motoric, and electrophysiological activity. Sleep-wake behavior of rats, rabbits, and human infants (3 of each species) was observed, and, at the same time, a single-channel analog recording was obtained of the motoric activity. A judge who had extensive experience in observing sleep-wake behaviors of human infants, but who was unfamiliar with these behaviors in nonhuman species, scored the analog signals of the rats and rabbits. Another judge, who knew rat and rabbit state behaviors well, but who had not had experience observing human infants, judged the states of the human infants from the analog signals. These judgments were evaluated by comparing them with the findings obtained from direct observation of the subjects. For the nine subjects, the correlations between the judges' scoring of the analog recording and direct observation ranged from 0.856 to 0.985. A more stringent criterion is to determine the exact agreement between judge and observer for each 10-s epoch during the observation. For the major states of active sleep and quiet sleep, the exact agreement ranged from 95.2 to 100%. The wake state was easily judged for rats (100% agreement) but was more difficult for rabbits and humans (59.9 and 66.7%, respectively). This ability to accurately score the state behavior of an unfamiliar species from an analog movement record alone represents a cross-species invariance in neuromotor organization. The critical parameters appear to be regularity or irregularity of respiration and the temporal distribution of gross motor movement.

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Functional characterization of human brown adipose tissue metabolism

Biochemical Journal ◽

10.1042/bcj20190464 ◽

2020 ◽

Vol 477 (7) ◽

pp. 1261-1286 ◽

Cited By ~ 3

Author(s):

Marie Anne Richard ◽

Hannah Pallubinsky ◽

Denis P. Blondin

Keyword(s):

Adipose Tissue ◽

Brown Adipose Tissue ◽

Functional Characterization ◽

Human Infants ◽

Positron Emission ◽

Brown Adipose ◽

Treatment Of Obesity ◽

And Function

Brown adipose tissue (BAT) has long been described according to its histological features as a multilocular, lipid-containing tissue, light brown in color, that is also responsive to the cold and found especially in hibernating mammals and human infants. Its presence in both hibernators and human infants, combined with its function as a heat-generating organ, raised many questions about its role in humans. Early characterizations of the tissue in humans focused on its progressive atrophy with age and its apparent importance for cold-exposed workers. However, the use of positron emission tomography (PET) with the glucose tracer [18F]fluorodeoxyglucose ([18F]FDG) made it possible to begin characterizing the possible function of BAT in adult humans, and whether it could play a role in the prevention or treatment of obesity and type 2 diabetes (T2D). This review focuses on the in vivo functional characterization of human BAT, the methodological approaches applied to examine these features and addresses critical gaps that remain in moving the field forward. Specifically, we describe the anatomical and biomolecular features of human BAT, the modalities and applications of non-invasive tools such as PET and magnetic resonance imaging coupled with spectroscopy (MRI/MRS) to study BAT morphology and function in vivo, and finally describe the functional characteristics of human BAT that have only been possible through the development and application of such tools.

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