Perchance to dream? Primordial motor activity patterns in vertebrates from fish to mammals: their prenatal origin, postnatal persistence during sleep, and pathological reemergence during REM sleep behavior disorder.

An overview is presented of the literature dealing with sleep-like motility and concomitant neuronal activity patterns throughout the life cycle in vertebrates, ectothermic as well as endothermic. Spontaneous, periodically modulated, neurogenic bursts of non-purposive movements are a universal feature of larval and prenatal behavior, which in endothermic animals (i.e.

Call it sleep -- what animals without backbones can tell us about the phylogeny of intrinsically generated neuromotor rhythms during early development.

A comprehensive overview is presented of the literature dealing with the development of sleep-like motility and neuronal activity patterns in non-vertebrate animals. it has been established that spontaneous, periodically modulated, neurogenic bursts of movement appear to be a universal feature of prenatal behavior. New empirical data are presented showing that such' seismic sleep' or 'rapid-body-movement' bursts in cuttlefish persist for some time after birth.

From neural plate to cortical arousal-a neuronal network theory of sleep derived from in vitro "model" systems for primordial patterns of spontaneous bioelectric activity in the vertebrate central nervous system.

In the early 1960s intrinsically generated widespread neuronal discharges were discovered to be the basis for the earliest motor behavior throughout the animal kingdom. The pattern generating system is in fact programmed into the developing nervous system, in a regionally specific manner, already at the early neural plate stage. Such rhythmically modulated phasic bursts were next discovered to be a general feature of developing neural networks and, largely on the basis of experimental interventions in cultured neural tissues, to contribute significantly to their morpho-physiological maturation.

Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling.

Cholinergic neuromodulation plays key roles in the regulation of neuronal excitability, network activity, arousal, and behavior. On longer time scales, cholinergic systems play essential roles in cortical development, maturation, and plasticity. Presumably, these processes are associated with substantial synaptic remodeling, yet to date, long-term relationships between cholinergic tone and synaptic remodeling remain largely unknown.

The sleep-like nature of early mammalian behavioral rhythms: Theoretical comment on Todd et al. (2010).

Early sleep patterns lack several of the major defining physiological criteria used to identify sleep states in adult animals, but many typical aspects of mature sleep can nevertheless be demonstrated at surprisingly early stages of development. In Todd, Gibson, Shaw, & Blumberg (2010), the ability to compensate for enforced sleep deprivation is found to be present already shortly after birth in laboratory rats, an altricial mammalian species. Whereas the brainstem is capable of resisting enforced wakefulness by an increasing "pressure" to fall asleep, "catch-up" replacement of the lost sleep by means of longer subsequent sleep durations requires forebrain participation.

Spontaneous neuronal burst discharges as dependent and independent variables in the maturation of cerebral cortex tissue cultured in vitro: a review of activity-dependent studies in live 'model' systems for the development of intrinsically generated bioelectric slow-wave sleep patterns.

A survey is presented of recent experiments which utilize spontaneous neuronal spike trains as dependent and/or independent variables in developing cerebral cortex cultures when synaptic transmission is interfered with for varying periods of time. Special attention is given to current difficulties in selecting suitable preparations for carrying out biologically relevant developmental studies, and in applying spike-train analysis methods with sufficient resolution to detect activity-dependent age and treatment effects. A hierarchy of synchronized nested burst discharges which approximate early slow-wave sleep patterns in the intact organism is established as a stable basis for isolated cortex function.

Physiological consequences of selective suppression of synaptic transmission in developing cerebral cortical networks in vitro: differential effects on intrinsically generated bioelectric discharges in a living 'model' system for slow-wave sleep activity.

Within the context of an updated thorough review of the literature concerning activity-dependent cerebro-cortical development, a survey is made of recent experiments which utilize spontaneous spike-trains as the dependent variable in rodent neocortex cultures when synaptic transmission is interfered with during early ontogeny. Emphasis is placed on the complexity of homeostatic adaptations to reduced as well as intensified firing. Two kinds of adaptation are distinguished: (i) rapid recovery (within several hours) towards baseline levels despite sustained blockade of excitatory synaptic transmission, and (ii) the generation of essentially normal firing patterns in cultures assayed in control medium following development in the presence of excitatory receptor blockers.

Reciprocal homeostatic responses to excitatory synaptic receptor inactivation in developing organotypic cortical networks in vitro.

Chronic blockade of actively excitatory glutamatergic synaptic receptors in co-cultured organotypic rodent neocortex explants rapidly leads to a compensatory sensitization of otherwise inactive input channels so as to maintain ongoing action potential bursts. We report here that the homeostatic return of spontaneous, kainate receptor driven, spike discharges is followed by a reciprocal desensitization of blocked AMPA and NMDA receptors, such that the developing network is protected against becoming hyperactive once full synaptic drive is restored.

Homeostatically regulated spontaneous neuronal discharges protect developing cerebral cortex networks from becoming hyperactive following prolonged blockade of excitatory synaptic receptors.

In order to further examine the role of spontaneous action potential (SAP) discharges in neocortical development, amino-acid-mediated synaptic transmission was selectively blocked in an improved organotypic neocortex culture preparation. Contralateral occipital cortex slices from neonatal rats were co-cultured for several weeks in a ventricle-to-ventricle orientation known to greatly enhance cyto-morphological and electrophysiological maturation. Such preparations are highly resistant to attempts to suppress neuronal firing by blocking ionotropic glutamate receptors: not only can kainate receptors partly substitute for NMDA- and AMPA-mediated neurotransmission when these receptors are pharmacologically blocked, but (muscarinic) cholinergic receptors also begin to drive SAP activity when the kainate receptors, too, are chronically blocked.

Spontaneous neuronal discharge patterns in developing organotypic mega-co-cultures of neonatal rat cerebral cortex.

Sagittal slices of neonatal rat neocortex, extending from the prefrontal to the occipital area, were cultured separately or in pairs, oriented in such a way that axons projecting from the ventricular surface of each explant could innervate the other one. Functional connections were made between as well as within the explants, and spontaneous field potentials and associated action potentials occurred in variable bursts, and with varying degrees of synchrony. Spike-train analysis revealed that the activity patterns seen in these 'mega' co-cultures closely mimic 'tracé alternant' patterns, consisting of trains of burst discharges recurring several times per minute, which are characteristic for the immature intact cerebral cortex during slow-wave sleep.

Compensatory physiological responses to chronic blockade of amino acid receptors during early development in spontaneously active organotypic cerebral cortex explants cultured in vitro.

Paired organotypic explants from rat occipital cortex were cultured for up to three weeks in the presence of selective blockers of amino acid receptor blockers, during which period spontaneous action potential generation was monitored electrophysiologically. In contrast to isolated explants (Corner, M.A.

Dynamics and plasticity in developing neuronal networks in vitro.

When dissociated cortical tissue is brought into culture, neurons readily grow out by forming axonal and dendritic arborizations and synaptic connections. These developing neuronal networks in vitro display spontaneous firing activity from about the end of the first week in vitro. When cultured on multielectrode arrays firing activity can be recorded from many neurons simultaneously over long periods of time.