Isolated rat pups respond to cold exposure physiologically by increasing metabolic heat production and behaviorally by emitting ultrasound. The relationship between these 2 responses was investigated by monitoring oxygen consumption, heat production by brown adipose tissue, respiratory rate, and ultrasound production during cold exposure in pups 10-12 days of age. All 3 physiological measures increased contemporaneously with the initiation of ultrasound. Pups also exhibited a respiratory pattern characterized by the prolongation of expiratory duration in relation to inspiratory duration. Ultrasound was often detected during these prolonged expirations, suggesting that pups were using laryngeal braking. Laryngeal braking is thought to enhance oxygen uptake in the lungs. Thus, ultrasound may be an acoustic by-product of a respiratory maneuver that increases oxygen delivery to metabolically active tissues during cold exposure.
Summary Spontaneous activity in the sensory periphery drives infant brain activity and is thought to contribute to the formation of retinotopic and somatotopic maps [1–3]. In infant rats during active (or REM) sleep, brainstem-generated spontaneous activity triggers hundreds of thousands of skeletal muscle twitches each day [4]; sensory feedback arising from the resulting limb movements is a primary activator of forebrain activity, including spindle bursts in somatosensory cortex [1]. The rodent whisker system, with its precise isomorphic mapping of individual whiskers to discrete brain areas, has been a key contributor to our understanding of somatotopic maps and developmental plasticity [5–7]. However, in contrast with other sensory systems—and even though whisker movements are controlled by dedicated skeletal muscles [8, 9]—spontaneous whisker activity has not been entertained as a contributing factor to the development of this system [10]. Here we report in 3- to 6-day-old rats that whiskers twitch rapidly and asynchronously during active sleep. In addition, neurons in whisker thalamus exhibit bursts of activity that are tightly associated with twitches, but occur infrequently during waking. Finally, we observed barrel-specific cortical activity during periods of twitching. This is the first report of self-generated, sleep-related twitches in the developing whisker system, a sensorimotor system that is unique for the precision with which it can be experimentally manipulated. Therefore, the discovery of whisker twitching will allow us to attain a fuller understanding of the contributions of peripheral sensory activity to somatosensory integration and plasticity in the developing nervous system [11–13].
] indicate that sleep bout durations exhibit an exponential distribution, whereas wake bout durations exhibit a power-law distribution. Moreover, it was found that wake bout distributions, but not sleep bout distributions, exhibit scale invariance across mammals of different body sizes. Here we test the generalizability of these findings by examining the distributions of sleep and wake bout durations in infant rats between 2 and 21 days of age. In agreement with Lo et al., we find that sleep bout durations exhibit exponential distributions at all ages examined. In contrast, however, wake bout durations also exhibit exponential distributions at the younger ages, with a clear power-law distribution only emerging at the older ages. Further analyses failed to find substantial evidence either of short-or long-term correlations in the data, thus suggesting that the durations of current sleep and wake bouts evolve through time without memory of the durations of preceding bouts. These findings further support the notion that bouts of sleep and wakefulness are regulated independently. Moreover, in light of recent evidence that developmental changes in sleep and wake bouts can be attributed in part to increasing forebrain influences, these findings suggest the possibility of identifying specific neural circuits that modulate the changing complexity of sleep and wake dynamics during development.atonia ͉ renewal process ͉ Markov process ͉ development A s members of a diurnal species, adult humans experience sleep as a prolonged period of rest during the night; however, sleep actually occurs as a series of discrete bouts interrupted by bouts of wakefulness. What is perhaps most striking during the first several months after birth, when circadian influences on behavioral state are not well established, is the brevity of these bouts of sleep and wakefulness (1). In newborn rats at 2 days of age (P2), these cycles are astonishingly rapid: The average bout lengths of nuchal muscle atonia (indicative of sleep) and high nuchal muscle tone (indicative of wakefulness) are only 15 s and 5 s, respectively (2). Over the next week, bout lengths increase significantly as forebrain mechanisms exert increasing modulatory control over brainstem mechanisms controlling sleep and wakefulness (2).Recently, Lo et al. (3) analyzed the distributions of sleep and wake bouts in human adults. They found that, whereas sleep bouts exhibited an exponential distribution [such that the frequency distribution f(t) of bout durations of duration t was proportional to e (Ϫt/) , where is the characteristic time scale], wake bouts exhibited a power-law distribution [such that f(t) Ϸ t Ϫ␣ , where ␣ is a characteristic power-law exponent]. In a subsequent report (4), these findings were extended to cats, rats, and mice. From this comparative analysis, Lo and colleagues found that the exponential time scale for sleep bout durations increased with body size, thus possibly implicating a constitutional variable (e.g., metabolic rate) in the regulation of sleep bout...
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.
Sleep is a poorly understood behavior that predominates during infancy but is studied almost exclusively in adults. One perceived impediment to investigations of sleep early in ontogeny is the absence of state-dependent neocortical activity. Nonetheless, in infant rats, sleep is reliably characterized by the presence of tonic (i.e., muscle atonia) and phasic (i.e., myoclonic twitching) components; the neural circuitry underlying these components, however, is unknown. Recently, we described a medullary inhibitory area (MIA) in week-old rats that is necessary but not sufficient for the normal expression of atonia. Here we report that the infant MIA receives projections from areas containing neurons that exhibit state-dependent activity. Specifically, neurons within these areas, including the subcoeruleus (SubLC), pontis oralis (PO), and dorsolateral pontine tegmentum (DLPT), exhibit discharge profiles that suggest causal roles in the modulation of muscle tone and the production of myoclonic twitches. Indeed, lesions in the SubLC and PO decreased the expression of muscle atonia without affecting twitching (resulting in “REM sleep without atonia”), whereas lesions of the DLPT increased the expression of atonia while decreasing the amount of twitching. Thus, the neural substrates of infant sleep are strikingly similar to those of adults, a surprising finding in light of theories that discount the contribution of supraspinal neural elements to sleep before the onset of state-dependent neocortical activity.
The neonatal hippocampus exhibits regularly recurring waves of synchronized neuronal activity in vitro. Because active sleep (AS), characterized by bursts of phasic motor activity in the form of myoclonic twitching, may provide conditions that are conducive to activity-dependent development of hippocampal circuits, we hypothesized that the waves of synchronous neuronal activity that have been observed in vitro would be associated with AS-related twitching. Using unanesthetized 1-to 12-d-old rats, we report here that the majority of neurons in CA1 and the dentate gyrus (DG) are significantly more active during AS than during either quiet sleep or wakefulness. Neuronal activity typically occurs in phasic bursts, during which most neurons are significantly cross-correlated both within and across the CA1 and DG fields. All AS-active neurons increase their firing rates during periods of myoclonic twitching of the limbs, and a subset of these neurons exhibit a burst of activity immediately after limb twitches, suggesting that the twitches themselves provide sensory feedback to the infant hippocampus, as occurs in the infant spinal cord and neocortex. Finally, the synchronous bursts of neuronal activity are coupled to the emergence of the AS-related hippocampal gamma rhythm during the first postnatal week, as well as the emergence of the AS-related theta rhythm during the second postnatal week. We hypothesize that the phasic motor events of active sleep provide the developing hippocampus with discrete sensory stimulation that contributes to the development and refinement of hippocampal circuits as well as the development of synchronized interactions between hippocampus and neocortex.
It is still not known how the “rudimentary” movements of fetuses and infants are transformed into the coordinated, flexible, and adaptive movements of adults. In addressing this important issue, we consider a behavior that has been perennially viewed as a functionless by-product of a dreaming brain: the jerky limb movements called myoclonic twitches. Recent work has identified the neural mechanisms that produce twitching as well as those that convey sensory feedback from twitching limbs to the spinal cord and brain. In turn, these mechanistic insights have helped inspire new ideas about the functional roles that twitching might play in the self-organization of spinal and supraspinal sensorimotor circuits. Striking support for these ideas is coming from the field of developmental robotics: When twitches are mimicked in robot models of the musculoskeletal system, basic neural circuitry self-organizes. Mutually inspired biological and synthetic approaches promise not only to produce better robots, but also to solve fundamental problems concerning the developmental origins of sensorimotor maps in the spinal cord and brain.
When delta activity emerges at P11, it integrates smoothly with periods of QS, as defined using electromyogram and behavioral criteria alone. Delta activity helps to refine estimates of QS duration but does not reflect a significant alteration of sleep-state organization. Rather, this organization is expressed much earlier in ontogeny as fluctuations in muscle tone and associated phasic motor activity.
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