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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

Sketch made for a lecture in 1961 at the Zoology department, Columbia University (New York City) showing: left—the limb/nerve deplantation experiment of Paul Weiss in the axolotl dorsal fin; middle—a frog tadpole showing the transections made at different CNS levels; right—outline of the early anuran neural plate illustrating the spontaneous motility patterns generated by isolated presumptive CNS fragments combined with mesoderm (see text and [6] for details).
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brainsci-03-00800-f001: Sketch made for a lecture in 1961 at the Zoology department, Columbia University (New York City) showing: left—the limb/nerve deplantation experiment of Paul Weiss in the axolotl dorsal fin; middle—a frog tadpole showing the transections made at different CNS levels; right—outline of the early anuran neural plate illustrating the spontaneous motility patterns generated by isolated presumptive CNS fragments combined with mesoderm (see text and [6] for details).

Mentions: Until the middle of the last century little attention was paid to the possibility of intrinsically generated neuronal activity being a ubiquitous feature of brain function and behavior. It was then reported, however, that axolotl neuromotor tissues deplanted into a dorsal fin could innervate and trigger complex movements in isolated, similarly deplanted limbs [2] (Figure 1). The paradigm shift that this discovery heralded was not widely appreciated but, at about the same time, it was discovered that “rapid eye” (REM) and other body movements occur spontaneously during sleep in humans and many other animals. This “third physiological state” turned out to be a widespread phenomenon that has its origin in neuronal discharges originating in the rostral hindbrain [3,4]. Within a decade, by taking advantage of the late development of sensory nerves in chick embryos, and subsequently employing surgical deafferentation to confirm the deduction of a “non-reflexogenic” origin within the central nervous system, the principle of spontaneous neuromotor discharges had been broadened to include the onset of motility in endothermic vertebrates [5].


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)

Sketch made for a lecture in 1961 at the Zoology department, Columbia University (New York City) showing: left—the limb/nerve deplantation experiment of Paul Weiss in the axolotl dorsal fin; middle—a frog tadpole showing the transections made at different CNS levels; right—outline of the early anuran neural plate illustrating the spontaneous motility patterns generated by isolated presumptive CNS fragments combined with mesoderm (see text and [6] for details).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

brainsci-03-00800-f001: Sketch made for a lecture in 1961 at the Zoology department, Columbia University (New York City) showing: left—the limb/nerve deplantation experiment of Paul Weiss in the axolotl dorsal fin; middle—a frog tadpole showing the transections made at different CNS levels; right—outline of the early anuran neural plate illustrating the spontaneous motility patterns generated by isolated presumptive CNS fragments combined with mesoderm (see text and [6] for details).
Mentions: Until the middle of the last century little attention was paid to the possibility of intrinsically generated neuronal activity being a ubiquitous feature of brain function and behavior. It was then reported, however, that axolotl neuromotor tissues deplanted into a dorsal fin could innervate and trigger complex movements in isolated, similarly deplanted limbs [2] (Figure 1). The paradigm shift that this discovery heralded was not widely appreciated but, at about the same time, it was discovered that “rapid eye” (REM) and other body movements occur spontaneously during sleep in humans and many other animals. This “third physiological state” turned out to be a widespread phenomenon that has its origin in neuronal discharges originating in the rostral hindbrain [3,4]. Within a decade, by taking advantage of the late development of sensory nerves in chick embryos, and subsequently employing surgical deafferentation to confirm the deduction of a “non-reflexogenic” origin within the central nervous system, the principle of spontaneous neuromotor discharges had been broadened to include the onset of motility in endothermic vertebrates [5].

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