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The Pyramidal Cell and Its Local-Circuit Internemom: a Hypothetical Unit of the Mammalian Cerebral Cortex

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The Pyramidal Cell and Its Local-Circuit Internemom: a Hypothetical Unit of the Mammalian Cerebral Cortex The Pyramidal Cell and its Local-Circuit Internemom: A Hypothetical Unit of the Mammalian Cerebral Cortex Miguel Marin-Padilla Department of Pathology Dartmouth Medical School Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/2/3/180/1755663/jocn.1990.2.3.180.pdf by guest on 18 May 2021 Abstract A pyramidal cell with five of its local-circuit interneurons model infers that the number of pyramidal cells contacted by (Cajal-Retzius, Martinotti, Cajal double-bouquet, basket, and each Idcircuit interneuron as well as the nunzk of synaptic chandelier cells), constitutes a distinct structural/functional as- contacts established with each one are elements acquired post- semblage of the mammalian neocortex. This pyramiWld- natally in response to individual needs. Thereby, the overall circuit neuronal assemblage is proposed herein as a basic three-dimensional distribution and extent of these pyramidal/ neocortical unit. This unit is shared by all mammals, embodies local-circuit neuronal assemblages should be species-specific, both specific structural as well as functional elements, and variable among individual of the same species, and able to constitutes an essential developmental building block of the adapt in response to environmental needs. The model intro- neocortex. In the model, the pyramidal cell represents a dis- duces a different approach, perhaps a new vantage point, for tinct, stable, projective, excitatory neuron that has remained the study of the basic structural organization of the mammalian essentially unchanged in the course of mammalian phylogeny. cerebral cortex. Relationships of the proposed model to cortical On the other hand, its localcircuit interneurons are more likely function in general and to learning behavior in particular are to be inhibitory and less stable, designed perhaps to adapt, and discussed. modify in response to environmental needs. The proposed INTRODUCTION comprehending the common basic cytoarchitecture of There are fundamental similarities as well as dissimilar- the mammalian neocortex. ities in the structural organization of the cerebral cortex The pyramidal cell represents the projective neuron (neocortex) among mammals. The establishment of a of the unit and the local-circuit interneurons are the common structural/functional unit may facilitate a com- intracortical modulators of its functional activity. Each parative study of the basic neocortical cytoarchitecture. interneuron establishes a specific type of synaptic con- Hypothetically, a pyramidal cell together with five of its tacts with a different compartment of the pyramidal cell. local-circuit interneurons (Cajal-Retzius, Martinotti, Cajal The pyramidal cell represents a relatively stable neuron double-bouquet, basket, and chandelier cells) is pro- that has remained essentially unchanged in the course posed as a fundamental building block of the mammalian of mammalian phylogeny. On the other hand, the inter- neocortex. This pyramidaVlocal-circuit neuronal assem- neurons are less stable cells that change or adapt in blage is shared by all mammals, and embodies specific response to environmental demands. structural as well as functional elements. Hence it con- The structural and functional interrelationships among stitutes a structuralhnctional neocortical unit. It is fur- the various components of this hypothetical neocortical ther proposed that the cytoarchitectural plan of the unit will be analyzed and described in this article. The mammalian neocortex is based on the sequential devel- development of some of its components (e.g., the pyra- opment of these units at various cortical levels. Cortical midal cell) will also be analyzed. The relevance of this units of this type may be found at layers V, IV, 111, and I1 unit to neocortical structural organization in general, and throughout the entire neocortex. It must be emphasized to neuronal plasticity and learning in particular, will be that the proposed unit is but a hypothetical one out of discussed. Statements such as “We have no explanation many other possible units. It has been selected because why the histology of the cerebral cortex is what it is” it is structurally simple, universal, and may be useful in (Braitenberg 1978), and “we have yet to achieve a uni- 180 Journal of Cognitive Neuroscience Volume 2, Number 3 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1990.2.3.180 by guest on 25 September 2021 versal theory of cortical organization” (Rakic and Singer 1988) will be challenged. MATEIUb.L AND METHOD To describe and define this pyramidalllocal-circuit neu- ronal unit, Golgi preparations of the human cerebral cortex from the author’s collection have been used (see Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/2/3/180/1755663/jocn.1990.2.3.180.pdf by guest on 18 May 2021 Journal‘s cover page). The collection has been gathered over many years and is comprised of autopsy material from the cerebral cortex of premature fetuses (26, 28, 30, 32, 36, and 38 weeks old), newborns, and young children (2, 4, and 8 months old). Prematurity, respira- tory distress syndrome, bronchopulmonary dysplasia, cerebral hemorrhages, and congenital malformations were among the causes of these infants demise. The collection is made up of thousands of 100- to 150-~m- thick rapid Golgi preparations ranging in staining quality Erom excellent to poor. The Golgi method permits limited but accurate glimpses of the nervous structure. It is possible, with time and perseverance, to study within such preparations the location, morphology, composition, and spatial inter- relationships of entire neuronal assemblages. Neurons, as well as fibers, from many well-stained areas can be extracted from these preparations and reproduced in camera lucida drawings. Drawings from many such views can then be assembled into large mosaics that are useful for the study and reproduction of the basic cytoarchitec- ture of any CNS region (Fig. 1). This unique feature has not been surpassed and is undoubtedly the main reason for the uninterrupted use of this old, classic method (Golgi 1873). Figure 1. Mosaic reconstruction of camera lucida drawings, from rapid Golgi preparations (see Journal‘s cover), illustrating the struc- ~ralorganization of the motor cortex of a newborn child and its fundamental neuronal types. The pial surface is at the top of the figure, and at the bottom there are few polymorphous neurons of layer Wb. The various sizes and locations of pyramidal cells and of THE PYRAMIDA.L/LOCAL-CIRCIJIT localcircuit interneurons (Cajal-Retzius, Martinotti, double-tufted, NEURONAL UNIT basket cells) of the motor cortex as well as their spatial interrelation- Although the model of hypothetical neocortical unit ships (neuronal assemblages) are illustrated at the Same magnilica- this tion to facilitate tkir comparative analysis. Layers I, 11 (a,b), III utilizes neurons of the human cerebral cortex, its basic (a,b,c), N,V, and VI as well as remnants of the still undifferentiated structural and functional features should be applicable cortical plate (CP) are also illustrated. Scale=100 pm. to all mammals. The structure, intracortical distribution, and organization of each of its neuronal components will Mammalian Pyramidal Neuron be described separately. Particular attention will be paid The to the special type of synaptic contacts established be- The pyramidal cell, the most distinctive neuron of the tween each local-circuit interneuron and a different com- mammalian neocortex, is.characterized by unique de- partment of the pyramidal cell as well as to their spatial velopmental, structural, and functional features (Cajal interrelationships. The role of this unit as a develop- 1911; Lorente de N6 1949; Marin-Padilla 1970a, 1971, mental building block of the basic cytoarchitecture of 1972, 1978, 1988; Marin-Padilla and Marin-Padilla 1982; the mammalian neocortex will be emphasized. A three- Feldman 1984). Pyramidal cells are distributed through- dimensional reconstruction of the proposed neocortical out the entire neocortex and represent -70-80% of all unit illustrating its overall structural organization and the its neurons. According to their size and cortical depth, intracortical interrelationships among its various com- four types of pyramidal cells are generally recognized: ponents is reproduced in Figure 2. giant cells of layer V, large cells of layers V and lower Marfn-Padillla 181 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1990.2.3.180 by guest on 25 September 2021 Figure 2. Stereo pair of cam- era lucida drawings illustrating the structural organization and the various components and their interrelationships of the pyramidaVlocal-circuit neocort- ical unit proposed herein. Each pair illustrates the stable giant motor pyramidal cell (layer V) of the unit and five of its asso- ciated local-circuit interneu- Tons, including a Cajal-Retzius Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/2/3/180/1755663/jocn.1990.2.3.180.pdf by guest on 18 May 2021 cell (C-R) of layer I, a Cajal double-bouquet cell (D) of layer 111, a Martinotti cell (M) of layer V, a basket cell (B) of layer V, and a chandelier cell (C) of layer V. The entire unit represents a basic neuronal as- semblage characteristic of the mammalian neocortex. For the purpose of improving its stereoscopic view, the follow- ing pyramidal neurons (stable cells of other units) have been added to the mosaic: another giant pyramidal cell of layer V, a large one of layer 1111,
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