Spatiotemporal Structure of REM Sleep Twitching Reveals Developmental Origins of Motor Synergies

Blumberg, Mark S.; Coleman, Cassandra M.; Gerth, Ashlynn I.; McMurray, Bob

doi:10.1016/j.cub.2013.08.055

Cited by 96 publications

(118 citation statements)

References 46 publications

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“…Such accounting entails the gating or cancelling of reafference from self-generated movements. However, for the development and maintenance of precise, integrated, and hierarchically organized sensorimotor maps [32], infants likely depend upon the conveyance of high-fidelity sensory information from self-generated limb movements to developing brain structures [33, 34]. Twitch movements may be particularly well suited to this task because, unlike wake movements, they are produced discretely against a background of muscle atonia, both of which enhance signal-to-noise ratio [19].…”

Section: Resultsmentioning

confidence: 99%

Self-Generated Movements with “Unexpected” Sensory Consequences

2014

Self Cite

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SUMMARY The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6–10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep—a behavioral state that predominates in early infancy [12–16]—neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected.

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Section: Resultsmentioning

confidence: 99%

Self-Generated Movements with “Unexpected” Sensory Consequences

2014

Self Cite

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“…In rats, the highest amount of twitching can be observed during the first two postnatal weeks [13], which coincides with a period of rapid growth [1] and the emergence of adult-like motor skills [14]. Twitches occur in all skeletal muscles that have been investigated thus far, including those that control the limbs and digits [5], eyes [15], and whiskers [16], and it has been estimated that newborn rats produce hundreds of thousands of twitches each day [17]. Because motor learning requires copious amounts of experience [18], the sheer quantity of twitches suggests that they serve an important role.…”

Section: An Ideal Movementmentioning

confidence: 99%

“…Produced only during active sleep, twitches occur when all skeletal muscles are atonic [19]. Also, although twitches can occur in rapid succession, they rarely happen simultaneously [5], further reinforcing their discrete nature. In contrast, wake movements are typically composed of continuous and simultaneous muscle activations.…”

Section: An Ideal Movementmentioning

confidence: 99%

“…Conventionally, sleep is thought of as a time of behavioral quiescence, but this could not be further from the truth, especially during early development. Indeed, skeletal muscles throughout the body twitch frequently during active sleep [5]. As muscles twitch and limbs move, tactile receptors and proprioceptors transmit signals to the brain (e.g., [6,7]).…”

Section: Introductionmentioning

confidence: 99%

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Myoclonic Twitching and Sleep-Dependent Plasticity in the Developing Sensorimotor System

Tiriac

Sokoloff

Blumberg

2015

Curr Sleep Medicine Rep

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As bodies grow and change throughout early development and across the lifespan, animals must develop, refine, and maintain accurate sensorimotor maps. Here we review evidence that myoclonic twitches—brief and discrete contractions of the muscles, occurring exclusively during REM (or active) sleep, that result in jerks of the limbs—help animals map their ever-changing bodies by activating skeletal muscles to produce corresponding sensory feedback, or reafference. First, we highlight the spatiotemporal characteristics of twitches. Second, we review findings in infant rats regarding the multitude of brain areas that are activated by twitches during sleep. Third, we discuss evidence demonstrating that the sensorimotor processing of twitches is different from that of wake movements; this state-related difference in sensorimotor processing provides perhaps the strongest evidence yet that twitches are uniquely suited to drive certain aspects of sensorimotor development. Finally, we suggest that twitching may help inform our understanding of neurodevelopmental disorders, perhaps even providing opportunities for their early detection and treatment.

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“…The fetus exhibits REMs and jerky motions and also has penile erections, 29,30 all things which also occur during REM sleep. 31,32 Body temperature is not well regulated during REM sleep, and the sensation of weight is strongly reduced, as in the fetal state. Anecdotally, the sleeping position most frequent among humans is the "fetal position".…”

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confidence: 99%

Negative correlation between gestation and sleep durations in mammals

Gonfalone¹

2016

OAAP

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Many studies of sleep have tempted to establish a relation between environmental, ecological, and physiological variables and sleep duration. This article establishes unambiguously that there is a negative correlation between gestation and sleep durations in mammals. Gestation offers the advantage that one species is characterized by a precise value of its gestation time, with relative small variations, and it is a quantity that can easily be measured. The duration of gestation is a parameter which differs from other parameters that have been used for comparison, such as weight, brain size, and predatory danger. The review of all relevant research articles clearly demonstrates that those mammals, which have longer gestation period, experience less sleep. Within the class of mammals, precocial mammals, capable of moving at birth, show a relatively short amount of rapid eye movement (REM) sleep (a unique phase of mammalian sleep) that does not vary much after birth, while altricial species with a short gestation that are relatively more dependent at birth adjust their amount of REM sleep after birth and show longer sleep duration in-line with the present findings. The essential data on which this result is obtained has been deduced from an extensive and attentive review of previously published articles on mammalian sleep and mammalian gestation, among others. In answering the question "Why does species with a shorter gestation period need more sleep?", many similarities in behavior between the fetal state and REM sleep state have been identified. Even if at birth all sensory organs are fully developed, their functions have not been exercised, and it is proposed that the amount of REM sleep may be the time needed to strengthen adaptation of the senses to the external world and its components, such as light, sound, contact, taste, odors, and particularly cold and gravity. The assumption proposed is that REM sleep is needed to compensate for the short gestation. It is a period for the brain to reorder and rearrange all sensations accumulated during wake and prepare for the following wake period, and that REM sleep is a carry over of the fetal state.

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Spatiotemporal Structure of REM Sleep Twitching Reveals Developmental Origins of Motor Synergies

Cited by 96 publications

References 46 publications

Self-Generated Movements with “Unexpected” Sensory Consequences

Self-Generated Movements with “Unexpected” Sensory Consequences

Myoclonic Twitching and Sleep-Dependent Plasticity in the Developing Sensorimotor System

Negative correlation between gestation and sleep durations in mammals

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