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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.

Corner MA - Brain Sci (2013)

Bottom Line: 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.In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development.Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

View Article: PubMed Central - PubMed

Affiliation: Netherlands Institute for Brain Research, Amsterdam, 1071-TC, The Netherlands. m.corner@hccnet.nl.

ABSTRACT
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. In particular, the level of spontaneous synchronized bursting is homeostatically regulated, and has the effect of constraining the development of excessive network excitability. After birth or hatching, this "slow-wave" activity pattern becomes sporadically suppressed in favor of sensory oriented "waking" behaviors better adapted to dealing with environmental contingencies. It nevertheless reappears periodically as "sleep" at several species-specific points in the diurnal/nocturnal cycle. Although this "default" behavior pattern evolves with development, its essential features are preserved throughout the life cycle, and are based upon a few simple mechanisms which can be both experimentally demonstrated and simulated by computer modeling. In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development. Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

No MeSH data available.


Related in: MedlinePlus

Different patterns of spontaneous field potentials or isolated spiking (A–C), and all-or-none evoked responses (D–F) in organotypic chick embryo cerebral hemisphere explants: oscillographically recorded in 1968 at the Albert Einstein College of Medicine, New York, NY, USA.
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brainsci-03-00800-f006: Different patterns of spontaneous field potentials or isolated spiking (A–C), and all-or-none evoked responses (D–F) in organotypic chick embryo cerebral hemisphere explants: oscillographically recorded in 1968 at the Albert Einstein College of Medicine, New York, NY, USA.

Mentions: Perhaps the earliest indication that cerebral slow-wave activity during sleep has a similar neurophysiological basis as RBM at the brainstem level came from organotypic cultures of embryonic chick forebrain tissue (Figure 6). After several days of growth in vitro, stereotyped field potentials began to appear spontaneously every few seconds, much as they do in ovo under the rate-limiting control of maturing glutamic acid enzymatic systems [44,45], culminating in intrinsically generated trains of amplitude modulated slow wave complexes which typically occur in variable cycles lasting on the order of several minutes [46]. Comparable “basic waveforms” in the intact infant rat neocortex during quiet sleep were shown to be associated with discrete burst-pause neuronal discharges [47], the endogenous origin of which was first demonstrated using dispersed cortical cell cultures [48], and thereafter has been repeatedly verified using either organotypic explants [49,50,51] or dissociated neurons cultured on multi-electrode grids [52,53,54,55]. Indeed, the basic underlying mechanisms—(1) spontaneous transmitter release, (2) recurrent excitatory connectivity, and (3) activity-dependent membrane refractoriness [13]—that were discovered for the brainstem and spinal cord [11,12,13,14,16,17,18,19>] are sufficient for mimicking network bursting even in single cortical cell micro-cultures forced to intensively innervate themselves autaptically [56]. Importantly, in addition, neocortical cultures have been shown to possess several biochemical and metabolic characteristics of slow-wave sleep in the intact organism [53].


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.

Corner MA - Brain Sci (2013)

Different patterns of spontaneous field potentials or isolated spiking (A–C), and all-or-none evoked responses (D–F) in organotypic chick embryo cerebral hemisphere explants: oscillographically recorded in 1968 at the Albert Einstein College of Medicine, New York, NY, USA.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4061857&req=5

brainsci-03-00800-f006: Different patterns of spontaneous field potentials or isolated spiking (A–C), and all-or-none evoked responses (D–F) in organotypic chick embryo cerebral hemisphere explants: oscillographically recorded in 1968 at the Albert Einstein College of Medicine, New York, NY, USA.
Mentions: Perhaps the earliest indication that cerebral slow-wave activity during sleep has a similar neurophysiological basis as RBM at the brainstem level came from organotypic cultures of embryonic chick forebrain tissue (Figure 6). After several days of growth in vitro, stereotyped field potentials began to appear spontaneously every few seconds, much as they do in ovo under the rate-limiting control of maturing glutamic acid enzymatic systems [44,45], culminating in intrinsically generated trains of amplitude modulated slow wave complexes which typically occur in variable cycles lasting on the order of several minutes [46]. Comparable “basic waveforms” in the intact infant rat neocortex during quiet sleep were shown to be associated with discrete burst-pause neuronal discharges [47], the endogenous origin of which was first demonstrated using dispersed cortical cell cultures [48], and thereafter has been repeatedly verified using either organotypic explants [49,50,51] or dissociated neurons cultured on multi-electrode grids [52,53,54,55]. Indeed, the basic underlying mechanisms—(1) spontaneous transmitter release, (2) recurrent excitatory connectivity, and (3) activity-dependent membrane refractoriness [13]—that were discovered for the brainstem and spinal cord [11,12,13,14,16,17,18,19>] are sufficient for mimicking network bursting even in single cortical cell micro-cultures forced to intensively innervate themselves autaptically [56]. Importantly, in addition, neocortical cultures have been shown to possess several biochemical and metabolic characteristics of slow-wave sleep in the intact organism [53].

Bottom Line: 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.In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development.Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

View Article: PubMed Central - PubMed

Affiliation: Netherlands Institute for Brain Research, Amsterdam, 1071-TC, The Netherlands. m.corner@hccnet.nl.

ABSTRACT
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. In particular, the level of spontaneous synchronized bursting is homeostatically regulated, and has the effect of constraining the development of excessive network excitability. After birth or hatching, this "slow-wave" activity pattern becomes sporadically suppressed in favor of sensory oriented "waking" behaviors better adapted to dealing with environmental contingencies. It nevertheless reappears periodically as "sleep" at several species-specific points in the diurnal/nocturnal cycle. Although this "default" behavior pattern evolves with development, its essential features are preserved throughout the life cycle, and are based upon a few simple mechanisms which can be both experimentally demonstrated and simulated by computer modeling. In contrast, a late onto- and phylogenetic aspect of sleep, viz., the intermittent "paradoxical" activation of the forebrain so as to mimic waking activity, is much less well understood as regards its contribution to brain development. Some recent findings dealing with this question by means of cholinergically induced "aroused" firing patterns in developing neocortical cell cultures, followed by quantitative electrophysiological assays of immediate and longterm sequelae, will be discussed in connection with their putative implications for sleep ontogeny.

No MeSH data available.


Related in: MedlinePlus