Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks

Rio-Bermudez, Carlos Del; Blumberg, Mark S.

doi:10.1002/bies.201700234

Cited by 56 publications

(42 citation statements)

References 79 publications

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“…A related issue is whether the sleep-inducing effect of SGRI caused synapse maturation, as opposed to a direct effect on ACx or thalamic inhibitory synapses. This is also a plausible hypothesis in that manipulations of sleep can influence CNS development (Miyamoto and Hensch, 2003;Peirano and Algarín, 2007;Frank, 2015;Del Rio-Bermudez and Blumberg, 2018). However, the literature showing that GABAergic signaling can have a direct effect on intracellular signaling and gene expression, discussed above, suggests that SGRI likely had a direct effect on GABAergic synapse maturation.…”

Section: Relationship Between Synaptic and Behavioral Findingsmentioning

confidence: 97%

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

Mowery¹,

Caras²,

Hassan³

et al. 2019

J. Neurosci.

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Transient periods of childhood hearing loss can induce deficits in aural communication that persist long after auditory thresholds have returned to normal, reflecting long-lasting impairments to the auditory CNS. Here, we asked whether these behavioral deficits could be reversed by treating one of the central impairments: reduction of inhibitory strength. Male and female gerbils received bilateral earplugs to induce a mild, reversible hearing loss during the critical period of auditory cortex development. After earplug removal and the return of normal auditory thresholds, we trained and tested animals on an amplitude modulation detection task. Transient developmental hearing loss induced both learning and perceptual deficits, which were entirely corrected by treatment with a selective GABA reuptake inhibitor (SGRI). To explore the mechanistic basis for these behavioral findings, we recorded the amplitudes of GABA A and GABA B receptor-mediated IPSPs in auditory cortical and thalamic brain slices. In hearing loss-reared animals, cortical IPSP amplitudes were significantly reduced within a few days of hearing loss onset, and this reduction persisted into adulthood. SGRI treatment during the critical period prevented the hearing loss-induced reduction of IPSP amplitudes; but when administered after the critical period, it only restored GABA B receptor-mediated IPSP amplitudes. These effects were driven, in part, by the ability of SGRI to upregulate ␣1 subunitdependent GABA A responses. Similarly, SGRI prevented the hearing loss-induced reduction of GABA A and GABA B IPSPs in the ventral nucleus of the medial geniculate body. Thus, by maintaining, or subsequently rescuing, GABAergic transmission in the central auditory thalamocortical pathway, some perceptual and cognitive deficits induced by developmental hearing loss can be prevented.

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Section: Relationship Between Synaptic and Behavioral Findingsmentioning

confidence: 97%

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

Mowery¹,

Caras²,

Hassan³

et al. 2019

J. Neurosci.

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“…Here, by deriving a novel theory, compiling comprehensive data on sleep and brain development, and quantitatively comparing sleep ontogeny with sleep phylogeny, we illuminate the dominant functions of sleep and how they change through development. Infants spend a much greater percentage of time in REM sleep compared with older children and adults.This finding suggests that REM sleep is likely crucial for the initial growth of babies, and perhaps especially for the regulation of synaptic weights throughout the nervous system(97). These substantial changes in percent REM sleep across human growth are in stark contrast with the constant percentage of REM sleep observed across an enormous range in brain and body size for adult mammals(42).…”

mentioning

confidence: 99%

Unraveling Why We Sleep: Quantitative Analysis Reveals Abrupt Transition from Neural Reorganization to Repair in Early Development

Cao

Herman

West

et al. 2019

Preprint

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Sleep serves disparate functions, most notably neural repair, metabolite clearance and circuit reorganization, yet the relative importance of these functions remains hotly debated. Here, we create a novel mechanistic framework for understanding and predicting how sleep changes during ontogeny (why babies sleep twice as long as adults) and across phylogeny (why mice sleep roughly five times that of whales). We use this theory to quantitatively distinguish between sleep used for neural reorganization versus repair. We conduct a comprehensive, quantitative analysis of human sleep using total sleep time, cere-bral metabolic rate, brain size, synaptic density, and REM sleep (used here to also refer to Active Sleep in infants and children). Our findings reveal an abrupt transition, between 2 and 3 years of age in humans. Specifically, our results show that differences in sleep across phylogeny and during late ontogeny (after 2 or 3 years in humans) are primarily due to sleep functioning for repair or clearance, while changes in sleep during early ontogeny (before 2 -3 years in humans) primarily support neural reorganization and learning. Moreover, our analysis shows that neuroplastic reorganization occurs primarily in REM sleep but not in NREM. In accordance with the developmental role of neuroplasticity, the percent of time spent in REM sleep is independent of brain size across species but decreases dramatically as brain size grows through development. Furthermore, the ratio of NREM sleep time to awake time emerges as a new invariant across development. This developmental transition and fundamental shift across ontogeny and phylogeny suggests a complex interplay between developmental and evolutionary constraints on sleep.

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“…This investigation of twitching in human infants, combined with recent advances in understanding the spatiotemporal dynamics and neurophysiological causes and consequences of twitching in infant rodents (Blumberg & Dooley, ; Del Rio‐Bermudez & Blumberg, ), leads us to believe that increased attention to sleep and sleep‐related twitching has the potential to open new avenues to understanding typical development. Such attention may also facilitate improved practices in neonatal intensive care units (NICUs), in which ambient conditions (e.g., lighting, sound) are often not conducive to sleep (Lai & Bearer, ).…”

Section: Discussionmentioning

confidence: 99%

“…High levels of active sleep in early development inspired, over 50 years ago, the hypothesis that active sleep is critical to brain development (Roffwarg et al, ). In the intervening years, developmental scientists have sought to identify the functions of active sleep and the mediating mechanisms involved (Blumberg, , ; Del Rio‐Bermudez & Blumberg, ; Frank, Issa, & Stryker, ; Marks, Shaffery, Oksenberg, Speciale, & Roffwarg, ; Mirmiran, ; Tarullo, Balsam, & Fifer, ). We posited that twitches exhibit features that, in contrast to wake movements, make them well‐suited to contribute to certain aspects of sensorimotor development (Blumberg, Marques, et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Such attention may also facilitate improved practices in neonatal intensive care units (NICUs), in which ambient conditions (e.g., lighting, sound) are often not conducive to sleep (Lai & Bearer, ). Given that sleep provides a critical context for sensory processing and functional connectivity in early development (Del Rio‐Bermudez & Blumberg, ; Del Rio‐Bermudez, Kim, Sokoloff, & Blumberg, ), minimizing sleep disturbances in the NICU could mitigate the negative effects of premature birth on sensory processing (Ryckman, Hilton, Rogers, & Pineda, ) and functional connectivity (Rogers, Lean, Wheelock, & Smyser, ).…”

Section: Discussionmentioning

confidence: 99%

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Spatiotemporal organization of myoclonic twitching in sleeping human infants

Sokoloff

Hickerson

Wen

et al. 2020

Developmental Psychobiology

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During the perinatal period in mammals when active sleep predominates, skeletal muscles twitch throughout the body. We have hypothesized that myoclonic twitches provide unique insight into the functional status of the human infant's nervous system. However, assessments of the rate and patterning of twitching have largely been restricted to infant rodents. Thus, here we analyze twitching in human infants over the first seven postnatal months. Using videography and behavioral measures of twitching during bouts of daytime sleep, we find at all ages that twitching across the body occurs predominantly in bursts at intervals of 10 s or less. We also find that twitching is expressed differentially across the body and with age. For example, twitching of the face and head is most prevalent shortly after birth and decreases over the first several months. In addition, twitching of the hands and feet occurs at a consistently higher rate than does twitching elsewhere in the body. Finally, the patterning of twitching becomes more structured with age, with twitches of the left and right hands and feet exhibiting the strongest coupling. Altogether, these findings support the notion that twitches can provide a unique source of information about typical and atypical sensorimotor development.

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Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks

Cited by 56 publications

References 79 publications

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

Unraveling Why We Sleep: Quantitative Analysis Reveals Abrupt Transition from Neural Reorganization to Repair in Early Development

Spatiotemporal organization of myoclonic twitching in sleeping human infants

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