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The Cajal School in the Peripheral Nervous System: The Transcendent Contributions of Fernando de Castro on the Microscopic Structure of Sensory and Autonomic Motor Ganglia.

de Castro F - Front Neuroanat (2016)

Bottom Line: Lawrentjew and the Spanish Fernando de Castro developed new technical approaches with spectacular results.In the mid of the 1920's, both young neuroscientists were worldwide recognized as the top experts in the field.Most of these discoveries remain fully alive today.

View Article: PubMed Central - PubMed

Affiliation: Grupo de Neurobiología del Desarrollo-GNDe, Instituto Cajal-CSIC Madrid, Spain.

ABSTRACT
The fine structure of the autonomic nervous system was largely unknown at the beginning of the second decade of the 20th century. Although relatively anatomists and histologists had studied the subject, even the assays by the great Russian histologist Alexander Dogiel and the Spanish Nobel Prize laureate, Santiago Ramón y Cajal, were incomplete. In a time which witnessed fundamental discoveries by Langley, Loewi and Dale on the physiology of the autonomic nervous system, both reputed researchers entrusted one of their outstanding disciples to the challenge to further investigate autonomic structures: the Russian B.I. Lawrentjew and the Spanish Fernando de Castro developed new technical approaches with spectacular results. In the mid of the 1920's, both young neuroscientists were worldwide recognized as the top experts in the field. In the present work we describe the main discoveries by Fernando de Castro in those years regarding the structure of sympathetic and sensory ganglia, the organization of the synaptic contacts in these ganglia, and the nature of their innervation, later materialized in their respective chapters, personally invited by the editor, in Wilder Penfield's famous textbook on Neurology and the Nervous System. Most of these discoveries remain fully alive today.

No MeSH data available.


Related in: MedlinePlus

Sympathetic neurons by Fernando de Castro. (A) de Castro’s hand-made schematic illustration of sympathetic neurons stained with the Cajal’s method, showing short long (a –the axón arises from this dendrite at a distance from the soma, c), short dendrites (b). This image was published in de Castro (1933). (B) Partial view of a sympathetic ganglion (normal condition) of an adult cow (de Castro, 1937). (C) Portion of a sympathetic ganglion with regenerated preganglionic fibers (a) after a vagus-sympathetic crossed anastomosis (de Castro, 1937; A) is part of Archive Fernando de Castro.
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Figure 3: Sympathetic neurons by Fernando de Castro. (A) de Castro’s hand-made schematic illustration of sympathetic neurons stained with the Cajal’s method, showing short long (a –the axón arises from this dendrite at a distance from the soma, c), short dendrites (b). This image was published in de Castro (1933). (B) Partial view of a sympathetic ganglion (normal condition) of an adult cow (de Castro, 1937). (C) Portion of a sympathetic ganglion with regenerated preganglionic fibers (a) after a vagus-sympathetic crossed anastomosis (de Castro, 1937; A) is part of Archive Fernando de Castro.

Mentions: Undoubtedly impelled by the success of his research on the histology of the human somatic sensory ganglia, as well as by the evident lack of studies with neurofibrillary methods at that time, Fernando de Castro re-assumed a research line which he briefly explored in the very first years of his scientific career (de Castro, 1916): a serious study of the histology of autonomic ganglia. This research line can be considered as completed with the publication of a monograph and a series of shorter articles which includes maybe the most important comparative study between mammalian species including primates and humans to that date (de Castro, 1923a,b, 1926, 1927), although important morpho-functional observations derive from works mainly devoted to other subjects than sympathetic ganglia (for details about the latter three studies, see below de Castro, 1932a,b, 1937, 1942; de Castro and Herreros, 1945; Figure 3). Together with research by other colleagues (Van Gehuchten, Lenhossek, Retzius, Köelliker, Cajal, Mihailov, etc.), de Castro’s contribution during 25 years of work in this field affirmed that the preganglionic connections wrap in spirals onto ganglionic cells to form the pericellular nests described by Ehrlich in the frog (although the number of these nests are largely lower in mammals; Ehrlich, 1888; de Castro, 1923a,b, 1932b). De Castro also affirmed that these dendritic nests, far from being accidental arrangements, are receptive sites for specific synaptic contacts from preganglionic fibers (de Castro, 1923b). Indeed, the fibers climbing along the dendrites, forming what they called the “receptive plaques”, were pointed by Cajal and de Castro as maybe the most frequent form of intercellular connection in the sympathetic ganglia (de Castro, 1923a,b, 1933, 1951). It was almost a decade after these first descriptions by de Castro that synapses were suggested to be present at the terminal boutons of the preganglionic fibers (de Castro, 1930, 1933; Lawrentjew, 1931, 1934a,b; Kolossow and Sabussow, 1932; Fedorow and Matwejewa, 1935; Bullón Ramirez, 1945; Bullón-Ramirez, 1947). These morphological descriptions contributed to the notion that three main types of neuron can be distinguished in the sympathetic motor ganglia (big, medium size and small neurons, big and small neurons each approximately 25% of the population, and medium size 50%). In each ganglion cells of these three types are intermingled and distributed in an apparent arbitrary way (de Castro, 1932b, 1937, 1950), and each type of preganglionic fiber contacts exclusively one type of ganglionic cell (Billingsley and Ranson, 1918; de Castro, 1923a, 1932a,b, 1937), which coincides with electrophysiological recordings showing four different potential waves in sympathetic ganglia (Bishop and Heinbecker, 1932; Eccles, 1935a,b,c). In this sense, de Castro’s observations on the nature of the axons of Dogiel’s Type II cells confirmed that they project either to other neurons within the same ganglia or in other neighbor ganglia, while they never end in the enteric mucosa. These observations confirmed previous reports (Dogiel, 1899; Ramón y Cajal, 1905; Billingsley and Ranson, 1918; de Castro, 1923b). Thus, the sensory nature of these fibers, as proposed originally by Dogiel, could be discarded. Posterior denervation studies demonstrated that the number of intraganglionic synapses is significantly larger than that of terminal boutons (de Castro and Herreros, 1945). In the latter article the positioning of the synaptic boutons close to astrocytes suggests the presence of what has been described at the turn of the 21st century as “tripartite synapses” (Araque et al., 1999; Perea et al., 2009). Developmental evidence drove de Castro to suggest that the apparent disorder and arbitrary distribution of ganglionic cells derive from germinative centers or spheres disseminated within the ganglia (de Castro, 1923a, 1932a,b). Although they appear in these studies as modest details, de Castro’s mind caught details here that remain uncontested and are still very important for our current perception of the structure and functioning of the nervous system. For example, he clearly stated that the ganglia are literally invaded by mesenchymal structures that lie interposed between the ganglionic neuronal components (somata, dendrites, axons). There always appeared to be a tiny glial mantle around neuronal components, forming a kind of “neuronal atmosphere”, for instance protecting axons once they loose their myelin sheaths (de Castro, 1937; de Castro and Herreros, 1945; Figure 3). In the ganglia the Schwann cells behave as the oligodendrocytes in the CNS, but de Castro also suggested that expansions emanated by Schwann cells form the intermediate portions of synapses, i.e., thin lamina interposed between the preganglionic fibers and the ganglionic neurons (de Castro, 1937; del Río-Hortega and Prado, 1941; de Castro, 1942; del Río-Hortega and Prado, 1942). It should be quoted here that de Castro, together with B.I. Lawrentjew, was among the first scientists specifically studying regeneration of synaptic contacts in the sympathetic system (Lawrentjew, 1925, 1934a,b; de Castro, 1930). In this series of scientific articles, de Castro showed in detail the cytoarchitecture of sympathetic and parasympathetic autonomic motor ganglia in humans, in other primates and in several large mammals. As a result of this research, de Castro was in 1924 awarded with the Martínez y Molina Prize (again from the Spanish Real Academia Nacional de Medicina). At that time the exhaustive and expert works of Fernando de Castro in the field of the histology of somatic sensory and autonomic ganglia had gained international recognition. The most clear example of this came by hand of the famous American neurosurgeon and neuropathologist Wilder S. Penfield (1891–1976), founder of the prestigious Montreal Neurological Institute (Canada): penfield invited de Castro to write two chapters for the first edition of his celebrated treaty “Penfield Cytology and Cellular Pathology of the Nervous System” (de Castro, 1932a,b). Penfield himself juicily described his “Quixotian adventure” (in his own words): his trip from the Presbyterian Hospital in New York, USA to 1924’s Madrid to work in the laboratory of Pío del Río-Hortega. In particular he describes his visit to Cajal’s laboratory on May 11th, to meet Cajal, Fernando de Castro and Domingo Sánchez:


The Cajal School in the Peripheral Nervous System: The Transcendent Contributions of Fernando de Castro on the Microscopic Structure of Sensory and Autonomic Motor Ganglia.

de Castro F - Front Neuroanat (2016)

Sympathetic neurons by Fernando de Castro. (A) de Castro’s hand-made schematic illustration of sympathetic neurons stained with the Cajal’s method, showing short long (a –the axón arises from this dendrite at a distance from the soma, c), short dendrites (b). This image was published in de Castro (1933). (B) Partial view of a sympathetic ganglion (normal condition) of an adult cow (de Castro, 1937). (C) Portion of a sympathetic ganglion with regenerated preganglionic fibers (a) after a vagus-sympathetic crossed anastomosis (de Castro, 1937; A) is part of Archive Fernando de Castro.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4837679&req=5

Figure 3: Sympathetic neurons by Fernando de Castro. (A) de Castro’s hand-made schematic illustration of sympathetic neurons stained with the Cajal’s method, showing short long (a –the axón arises from this dendrite at a distance from the soma, c), short dendrites (b). This image was published in de Castro (1933). (B) Partial view of a sympathetic ganglion (normal condition) of an adult cow (de Castro, 1937). (C) Portion of a sympathetic ganglion with regenerated preganglionic fibers (a) after a vagus-sympathetic crossed anastomosis (de Castro, 1937; A) is part of Archive Fernando de Castro.
Mentions: Undoubtedly impelled by the success of his research on the histology of the human somatic sensory ganglia, as well as by the evident lack of studies with neurofibrillary methods at that time, Fernando de Castro re-assumed a research line which he briefly explored in the very first years of his scientific career (de Castro, 1916): a serious study of the histology of autonomic ganglia. This research line can be considered as completed with the publication of a monograph and a series of shorter articles which includes maybe the most important comparative study between mammalian species including primates and humans to that date (de Castro, 1923a,b, 1926, 1927), although important morpho-functional observations derive from works mainly devoted to other subjects than sympathetic ganglia (for details about the latter three studies, see below de Castro, 1932a,b, 1937, 1942; de Castro and Herreros, 1945; Figure 3). Together with research by other colleagues (Van Gehuchten, Lenhossek, Retzius, Köelliker, Cajal, Mihailov, etc.), de Castro’s contribution during 25 years of work in this field affirmed that the preganglionic connections wrap in spirals onto ganglionic cells to form the pericellular nests described by Ehrlich in the frog (although the number of these nests are largely lower in mammals; Ehrlich, 1888; de Castro, 1923a,b, 1932b). De Castro also affirmed that these dendritic nests, far from being accidental arrangements, are receptive sites for specific synaptic contacts from preganglionic fibers (de Castro, 1923b). Indeed, the fibers climbing along the dendrites, forming what they called the “receptive plaques”, were pointed by Cajal and de Castro as maybe the most frequent form of intercellular connection in the sympathetic ganglia (de Castro, 1923a,b, 1933, 1951). It was almost a decade after these first descriptions by de Castro that synapses were suggested to be present at the terminal boutons of the preganglionic fibers (de Castro, 1930, 1933; Lawrentjew, 1931, 1934a,b; Kolossow and Sabussow, 1932; Fedorow and Matwejewa, 1935; Bullón Ramirez, 1945; Bullón-Ramirez, 1947). These morphological descriptions contributed to the notion that three main types of neuron can be distinguished in the sympathetic motor ganglia (big, medium size and small neurons, big and small neurons each approximately 25% of the population, and medium size 50%). In each ganglion cells of these three types are intermingled and distributed in an apparent arbitrary way (de Castro, 1932b, 1937, 1950), and each type of preganglionic fiber contacts exclusively one type of ganglionic cell (Billingsley and Ranson, 1918; de Castro, 1923a, 1932a,b, 1937), which coincides with electrophysiological recordings showing four different potential waves in sympathetic ganglia (Bishop and Heinbecker, 1932; Eccles, 1935a,b,c). In this sense, de Castro’s observations on the nature of the axons of Dogiel’s Type II cells confirmed that they project either to other neurons within the same ganglia or in other neighbor ganglia, while they never end in the enteric mucosa. These observations confirmed previous reports (Dogiel, 1899; Ramón y Cajal, 1905; Billingsley and Ranson, 1918; de Castro, 1923b). Thus, the sensory nature of these fibers, as proposed originally by Dogiel, could be discarded. Posterior denervation studies demonstrated that the number of intraganglionic synapses is significantly larger than that of terminal boutons (de Castro and Herreros, 1945). In the latter article the positioning of the synaptic boutons close to astrocytes suggests the presence of what has been described at the turn of the 21st century as “tripartite synapses” (Araque et al., 1999; Perea et al., 2009). Developmental evidence drove de Castro to suggest that the apparent disorder and arbitrary distribution of ganglionic cells derive from germinative centers or spheres disseminated within the ganglia (de Castro, 1923a, 1932a,b). Although they appear in these studies as modest details, de Castro’s mind caught details here that remain uncontested and are still very important for our current perception of the structure and functioning of the nervous system. For example, he clearly stated that the ganglia are literally invaded by mesenchymal structures that lie interposed between the ganglionic neuronal components (somata, dendrites, axons). There always appeared to be a tiny glial mantle around neuronal components, forming a kind of “neuronal atmosphere”, for instance protecting axons once they loose their myelin sheaths (de Castro, 1937; de Castro and Herreros, 1945; Figure 3). In the ganglia the Schwann cells behave as the oligodendrocytes in the CNS, but de Castro also suggested that expansions emanated by Schwann cells form the intermediate portions of synapses, i.e., thin lamina interposed between the preganglionic fibers and the ganglionic neurons (de Castro, 1937; del Río-Hortega and Prado, 1941; de Castro, 1942; del Río-Hortega and Prado, 1942). It should be quoted here that de Castro, together with B.I. Lawrentjew, was among the first scientists specifically studying regeneration of synaptic contacts in the sympathetic system (Lawrentjew, 1925, 1934a,b; de Castro, 1930). In this series of scientific articles, de Castro showed in detail the cytoarchitecture of sympathetic and parasympathetic autonomic motor ganglia in humans, in other primates and in several large mammals. As a result of this research, de Castro was in 1924 awarded with the Martínez y Molina Prize (again from the Spanish Real Academia Nacional de Medicina). At that time the exhaustive and expert works of Fernando de Castro in the field of the histology of somatic sensory and autonomic ganglia had gained international recognition. The most clear example of this came by hand of the famous American neurosurgeon and neuropathologist Wilder S. Penfield (1891–1976), founder of the prestigious Montreal Neurological Institute (Canada): penfield invited de Castro to write two chapters for the first edition of his celebrated treaty “Penfield Cytology and Cellular Pathology of the Nervous System” (de Castro, 1932a,b). Penfield himself juicily described his “Quixotian adventure” (in his own words): his trip from the Presbyterian Hospital in New York, USA to 1924’s Madrid to work in the laboratory of Pío del Río-Hortega. In particular he describes his visit to Cajal’s laboratory on May 11th, to meet Cajal, Fernando de Castro and Domingo Sánchez:

Bottom Line: Lawrentjew and the Spanish Fernando de Castro developed new technical approaches with spectacular results.In the mid of the 1920's, both young neuroscientists were worldwide recognized as the top experts in the field.Most of these discoveries remain fully alive today.

View Article: PubMed Central - PubMed

Affiliation: Grupo de Neurobiología del Desarrollo-GNDe, Instituto Cajal-CSIC Madrid, Spain.

ABSTRACT
The fine structure of the autonomic nervous system was largely unknown at the beginning of the second decade of the 20th century. Although relatively anatomists and histologists had studied the subject, even the assays by the great Russian histologist Alexander Dogiel and the Spanish Nobel Prize laureate, Santiago Ramón y Cajal, were incomplete. In a time which witnessed fundamental discoveries by Langley, Loewi and Dale on the physiology of the autonomic nervous system, both reputed researchers entrusted one of their outstanding disciples to the challenge to further investigate autonomic structures: the Russian B.I. Lawrentjew and the Spanish Fernando de Castro developed new technical approaches with spectacular results. In the mid of the 1920's, both young neuroscientists were worldwide recognized as the top experts in the field. In the present work we describe the main discoveries by Fernando de Castro in those years regarding the structure of sympathetic and sensory ganglia, the organization of the synaptic contacts in these ganglia, and the nature of their innervation, later materialized in their respective chapters, personally invited by the editor, in Wilder Penfield's famous textbook on Neurology and the Nervous System. Most of these discoveries remain fully alive today.

No MeSH data available.


Related in: MedlinePlus