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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

Two examples of “Frankensteinian” preparations prepared and filmed in 1961 at the Hubrecht International Embryology Laboratory in Utrecht, The Netherlands, consisting of anuran neural plate tissue, plus mesoderm, encased in a transparent ball of ectoderm. Differentiated CNS fragments (N) are covered by a pigment layer, and twitches of the muscle fibers (M) could be easily followed through a stereo microscope.
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brainsci-03-00800-f002: Two examples of “Frankensteinian” preparations prepared and filmed in 1961 at the Hubrecht International Embryology Laboratory in Utrecht, The Netherlands, consisting of anuran neural plate tissue, plus mesoderm, encased in a transparent ball of ectoderm. Differentiated CNS fragments (N) are covered by a pigment layer, and twitches of the muscle fibers (M) could be easily followed through a stereo microscope.

Mentions: In vitro culture techniques soon opened the way to an extension of this new paradigm to exothermic vertebrates [6]. Pieces of amphibian neural plate destined to become motor areas (Figure 1) could, when combined with presumptive muscle tissue and enclosed within an epithelial sheath (Figure 2), differentiate into central nervous structures that triggered spontaneous phasic contractions that were readily visible under the microscope. The addition of presumptive primary sensory neurons to these “Frankenstein models” for motorically active sleep although making possible the development of cutaneous reflex arcs, had no noticeable effect on the contractions, while presumptive forebrain areas failed altogether to support the appearance of either spontaneous or evoked twitching [7]. Indeed, the prosencephalic area of the plate was already “determined” (i.e., programmed for self-differentiation) to generate only forebrain structures such as retina, tapetum and olfactory placodes [9]. Micro-electrode recordings from neural plate derived hindbrain andspinalcord cultures [10] confirmed that a stereotyped phasic episode of polyneuronal firing immediately preceded each burst of contractions (Figure 3).


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)

Two examples of “Frankensteinian” preparations prepared and filmed in 1961 at the Hubrecht International Embryology Laboratory in Utrecht, The Netherlands, consisting of anuran neural plate tissue, plus mesoderm, encased in a transparent ball of ectoderm. Differentiated CNS fragments (N) are covered by a pigment layer, and twitches of the muscle fibers (M) could be easily followed through a stereo microscope.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

brainsci-03-00800-f002: Two examples of “Frankensteinian” preparations prepared and filmed in 1961 at the Hubrecht International Embryology Laboratory in Utrecht, The Netherlands, consisting of anuran neural plate tissue, plus mesoderm, encased in a transparent ball of ectoderm. Differentiated CNS fragments (N) are covered by a pigment layer, and twitches of the muscle fibers (M) could be easily followed through a stereo microscope.
Mentions: In vitro culture techniques soon opened the way to an extension of this new paradigm to exothermic vertebrates [6]. Pieces of amphibian neural plate destined to become motor areas (Figure 1) could, when combined with presumptive muscle tissue and enclosed within an epithelial sheath (Figure 2), differentiate into central nervous structures that triggered spontaneous phasic contractions that were readily visible under the microscope. The addition of presumptive primary sensory neurons to these “Frankenstein models” for motorically active sleep although making possible the development of cutaneous reflex arcs, had no noticeable effect on the contractions, while presumptive forebrain areas failed altogether to support the appearance of either spontaneous or evoked twitching [7]. Indeed, the prosencephalic area of the plate was already “determined” (i.e., programmed for self-differentiation) to generate only forebrain structures such as retina, tapetum and olfactory placodes [9]. Micro-electrode recordings from neural plate derived hindbrain andspinalcord cultures [10] confirmed that a stereotyped phasic episode of polyneuronal firing immediately preceded each burst of contractions (Figure 3).

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