Electron microscopy of the somatic sensory cortex of the cat III. The fine structure layers III to VI

Variations in the fine structure of layers III to VI of the somatic sensory cortex have been described. Layers III and IV may be readily distinguished from one another and from layers V and VI, but within the latter two layers there is such a slow gradient of change that no clear-cut line of junction can be drawn between them. Layer III is characterized by the presence of many large apical dendrites ascending vertically through it from pyramidal cells in all layers to reach layer I. In parallel with these are many small unmyelinated axons which contain flattened synaptic vesicles and terminate on transversely orientated dendrites in symmetrical synaptic complexes. The remainder of the neuropil is filled by large numbers of dendritic spines receiving axon terminals which contain spherical vesicles and which terminate asymmetrically. In layer IV there is a marked increase in the number of small myelinated axons ascending from below and ramifying within it. Embedded in the neuropil among these are many small non-pyramidal neurons whose somata and small, irregular dendrites are covered in axon terminals. Also present, and particularly concentrated at the junction with layer III, is a meshwork of fine unmyelinated axons which contain flattened vesicles and terminate in an en passant manner as symmetrical type synapses. Most of these axons are orientated transversely. A larger axon terminal which ends in asymmetrical complexes on small dendritic shafts and spines and which may be the terminal of thalamo-cortical axons is only found in any quantity in this layer. On descending into layers V and VI there is a progressive increase in the number of large myelinated fibres and glial cells, and a progressive diminution of neuronal elements, particularly dendritic spines. Some large non-pyramidal cells resembling the smaller ones on layer IV are present in layer VI.

Layers I and II of the somatic sensory cortex are clearly distinguishable with the electron microscope because of characteristic differences in the number, type and orientation of neurons and dendritic and axonal ramifications. Layer I may be subdivided into: (i) a subpial astrocytic layer immediately deep to the basement membrane of the cerebral surface; (ii) a superficial quarter consisting of bundles of small myelinated axons and large numbers of small axon terminals which contain spherical vesicles and end in asymmetrical synaptic complexes mainly on large dendritic spines. Most of these terminals are derived from a dense feltwork of fine unmyelinated axons which are especially concentrated at the junction of the superficial and deep parts of layer I; (iii) a deeper three quarters with similar features to the above but with the additional characteristic of many obliquely orientated large dendrites which are the diverging branches of apical dendrites ascending from deeper layers. Small pyramidal neurons dominate layer II, but among them are a small number of non-pyramidal neurons whose beaded dendrites are covered with axon terminals. Large apical dendrites traverse this layer, and in addition to the typical asymmetrical synapse on dendritic spines, a few symmetrical types appear. These are derived from thin unmyelinated axons orientated horizontally within the layer, and the terminals contain many small flattened or pleomorphic synaptic vesicles.


Two main types of neuron may be distinguished electron microscopically in the somatic sensory cortex. Pyramidal neurons have a characteristically triangular perikaryon with a high content of ribonucleoprotein consisting mainly of free ribosomes; the nucleus usually shows a single small indentation. Nonpyramidal neurons, which may be large or small, have a higher concentration of all intracytoplasmic organelles and particularly of long cisternae of rough-surfaced endoplasmic reticulum forming Nissl bodies. The nucleus is often deeply indented and crenellated. The two cell types differ also in the nature of their dendritic ramifications and particularly in their synaptic relationships. The majority of axon terminals ending on pyramidal neurons contact dendritic spines and relatively few end on the shafts of dendrites or on the perikaryon. Synapses on spines are typically of the type in which the synaptic thickenings are asymmetrical and the synaptic vesicles spherical. Such synapses, even when they occur on the shafts of pyramidal cell dendrites, are usually associated with a ‘spine apparatus’. Most of the few synapses on the dendritic shafts and somata of pyramidal cells are associated with symmetrical membrane contacts and small, flattened or pleomorphic vesicles. Terminals of this type are commonly en passant endings of long, thin unmyelinated axons oriented vertically or transversely within the cortex. The somata and the usually irregular dendrites of non-pyramidal neurons are typically covered in axon terminals most of which contain flattened vesicles and end in symmetrical complexes, but a few may contain spherical vesicles and end asymmetrically. The axon hillocks and initial segments of both types of cell are postsynaptic to axon terminals containing small, flattened vesicles and ending symmetrically.


2014 ◽  
Vol 112 (2) ◽  
pp. 263-275 ◽  
Author(s):  
Hayley A. Mattison ◽  
Ashish A. Bagal ◽  
Michael Mohammadi ◽  
Nisha S. Pulimood ◽  
Christian G. Reich ◽  
...  

GluA2-lacking, calcium-permeable α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors (AMPARs) have unique properties, but their presence at excitatory synapses in pyramidal cells is controversial. We have tested certain predictions of the model that such receptors are present in CA1 cells and show here that the polyamine spermine, but not philanthotoxin, causes use-dependent inhibition of synaptically evoked excitatory responses in stratum radiatum, but not s. oriens, in cultured and acute hippocampal slices. Stimulation of single dendritic spines by photolytic release of caged glutamate induced an N-methyl-d-aspartate receptor-independent, use- and spermine-sensitive calcium influx only at apical spines in cultured slices. Bath application of glutamate also triggered a spermine-sensitive influx of cobalt into CA1 cell dendrites in s. radiatum. Responses of single apical, but not basal, spines to photostimulation displayed prominent paired-pulse facilitation (PPF) consistent with use-dependent relief of cytoplasmic polyamine block. Responses at apical dendrites were diminished, and PPF was increased, by spermine. Intracellular application of pep2m, which inhibits recycling of GluA2-containing AMPARs, reduced apical spine responses and increased PPF. We conclude that some calcium-permeable, polyamine-sensitive AMPARs, perhaps lacking GluA2 subunits, are present at synapses on apical dendrites of CA1 pyramidal cells, which may allow distinct forms of synaptic plasticity and computation at different sets of excitatory inputs.


2020 ◽  
Vol 1 (1) ◽  
Author(s):  
Mamen Regalado-Reyes ◽  
Ruth Benavides-Piccione ◽  
Isabel Fernaud-Espinosa ◽  
Javier DeFelipe ◽  
Gonzalo León-Espinosa

Abstract The dendritic spines of pyramidal cells are the main postsynaptic target of excitatory glutamatergic synapses. Morphological alterations have been described in hippocampal dendritic spines during hibernation—a state of inactivity and metabolic depression that occurs via a transient neuronal tau hyperphosphorylation. Here, we have used the hibernating Syrian hamster to investigate the effect of hyperphosphorylated tau regarding neocortical neuronal structure. In particular, we examined layer Va pyramidal neurons. Our results indicate that hibernation does not promote significant changes in dendritic spine density. However, tau hyperphosphorylated neurons show a decrease in complexity, an increase in the tortuosity of the apical dendrites, and an increase in the diameter of the basal dendrites. Tau protein hyperphosphorylation and aggregation have been associated with loss or alterations of dendritic spines in neurodegenerative diseases, such as Alzheimer’s disease (AD). Our results may shed light on the correlation between tau hyperphosphorylation and the neuropathological processes in AD. Moreover, we observed changes in the length and area of the apical and basal dendritic spines during hibernation regardless of tau hyperphosphorylation. The morphological changes observed here also suggest region specificity, opening up debate about a possible relationship with the differential brain activity registered in these regions in previous studies.


1977 ◽  
Vol 25 (1) ◽  
pp. 1 ◽  
Author(s):  
CFL Hinrichsen ◽  
GE Stevens

Electron micrographs of sections of mouse neocortical layer IV, cut tangential to the pial surface, show the detailed organization of neuronal groups or 'barrels', which are related functionally to single facial vibrissae. Cortical barrels comprise 'sides' of stellate and small pyramidal neurons, groups of myelinated axons, and apical dendrites. The 'cores' comprise a neuropil of thalamic afferents, sparse neurons, converging basal dendrites of pyramidal cells and stellate cell dendrites. Some neurons of the 'sides' are attached through puncta adherentia.


2018 ◽  
Author(s):  
Guy Eyal ◽  
Matthias B. Verhoog ◽  
Guilherme Testa-Silva ◽  
Yair Deitcher ◽  
Ruth Benavides-Piccione ◽  
...  

AbstractWe present the first-ever detailed models of pyramidal cells from human neocortex, including models on their excitatory synapses, dendritic spines, dendritic NMDA- and somatic/axonal- Na+ spikes that provided new insights into signal processing and computational capabilities of these principal cells. Six human layer 2 and layer 3 pyramidal cells (HL2/L3 PCs) were modeled, integrating detailed anatomical and physiological data from both fresh and post mortem tissues from human temporal cortex. The models predicted particularly large AMPA- and NMDA- conductances per synaptic contact (0.88 nS and 1.31nS, respectively) and a steep dependence of the NMDA-conductance on voltage. These estimates were based on intracellular recordings from synaptically-connected HL2/L3 pairs, combined with extra-cellular current injections and use of synaptic blockers. A large dataset of high-resolution reconstructed HL2/L3 dendritic spines provided estimates for the EPSPs at the spine head (12.7 ± 4.6 mV), spine base (9.7 ± 5.0 mV) and soma (0.3 ± 0.1 mV), and for the spine neck resistance (50 – 80 MΩ). Matching the shape and firing pattern of experimental somatic Na+-spikes provided estimates for the density of the somatic/axonal excitable membrane ion channels, predicting that 134 ± 28 simultaneously activated HL2/L3- HL2/L3 synapses are required for generating (with 50% probability) a somatic Na+ spike. Dendritic NMDA spikes were triggered in the model when 20 ± 10 excitatory spinous synapses were simultaneously activated on individual dendritic branches. The particularly large number of basal dendrites in HL2/L3 PCs and the distinctive cable elongation of their terminals imply that ~25 NMDA- spikes could be generated independently and simultaneously in these cells, as compared to ~14 in L2/3 PCs from the rat temporal cortex. These multi-sites nonlinear signals, together with the large (~30,000) excitatory synapses/cell, equip human L2/L3 PCs with enhanced computational capabilities. Our study provides the most comprehensive model of any human neuron to-date demonstrating the biophysical and computational distinctiveness of human cortical neurons.


1969 ◽  
Vol 5 (2) ◽  
pp. 495-507
Author(s):  
E. G. JONES ◽  
T. P. S. POWELL

The axon hillocks and initial segments of pyramidal cell axons can be clearly recognized in electron micrographs of the somatic sensory cortex. The initial segment is characterized by three features: bundles of neurotubules linked together by electron-dense bands, a layer of dense material attached to the inner surface of the plasma membrane, and small membrane-bound dense bodies. All of these elements and the few ribosomes usually present disappear at the commencement of the myelin sheath. The initial segment of the axon often contains a cluster of cisternae similar to the spine apparatus, and this part of the axon sometimes gives off small branches. Axon terminals end on both the axon hillock and the initial segment, and there is an increase in number on the latter as the distance from the hillock increases. All of these terminals are relatively large, contain a high proportion of small flattened or pleomorphic synaptic vesicles and terminate in symmetrical synaptic contacts. These morphological features suggest that the synapses may be inhibitory in function.


1969 ◽  
Vol 5 (2) ◽  
pp. 509-529
Author(s):  
E. G. JONES ◽  
T. P. S. POWELL

The structural variations which occur in the dendritic spines of pyramidal neurons of the somatic sensory cortex of the cat are described, particular attention being paid to spines attached to different parts of the dendritic tree. Spines may be recognized particularly by the absence of neurotubules and the common presence of a spine apparatus, and they can be considered as pedunculated or sessile, depending upon the presence or absence of a narrow pedicle. Within these 2 categories spines may be rounded, cup-like or prismatic, can be large or small, and may show various degrees of inversion of the surface receiving a synaptic contact. While spines of every size and shape may be attached to dendrites of all diameters, there is a definite tendency for the largest spines to occur on the smallest dendrites and vice versa. Furthermore, the smallest dendrites possess the spines with the longest pedicles. Every dendritic spine receives 1 axon terminal containing spherical synaptic vesicles and ending in an asymmetrical synaptic contact. In addition, 10-20% of the spines receive a second terminal, which in some cases may contain spherical vesicles and terminate asymmetrically but in others contains small, flattened or pleomorphic vesicles and ends in a symmetrical contact. The additional terminal may end on the pedicle of the spine or on the parent dendrite near the attachment of the pedicle. In the latter site, asymmetrical synapses are commonly associated with an additional spine apparatus.


An experimental electron microscope (e.m.) study has been made of the termination of the afferent connections to the primate sensori-motor cortex. Following large, stereotaxically placed thalamic lesions, degeneration in the motor and somatic sensory cortices was studied at survival periods of 4 and 5 days. Degenerating thalamocortical terminals had asymmetric membrane specializations. In the motor cortex 89.5% made synapses on to dendritic spines, 9% on to dendritic shafts and 1.5% on to cell somata; in the somatic sensory area 89% made synapses on to spines, 11 % on to dendritic shafts and one example contacted a cell soma and a spine. A considerable number of the spines receiving synapses from degenerating thalamo-cortical terminals were traced to their parent dendrites and these were of the pyramidal type whereas the dendritic shafts and cell somata contacted by degenerating thalamo-cortical terminals were mostly of the large stellate type. Most of the thalamo-cortical degeneration in both cortical areas occurred in a dense band in the upper two thirds of layer IV and the lower half of layer III but a number of degenerating terminals were found deep to this; in the motor cortex a second, less dense, band of degeneration was present in the lower part of layer V and top of layer VI. Degenerating thalamo-cortical terminals making synapses on to dendritic shafts and cell somata were scattered through the deep half of the cortex and not concentrated in the dense band of degeneration and so formed a greater proportion of the degeneration in the deep layers, particularly in the motor cortex. Sections cut parallel to the pial surface in layer IV of the motor cortex showed a statistically significant association between the degenerating thalamocortical axon terminals and the bundles of apical dendrites present at this level. Degeneration of commissural fibres was studied after removal of the contralateral sensori-motor cortex. Degenerating terminals had asymmetric membrane specializations. In the motor cortex 96% made synapses on to dendritic spines, 3% contacted dendritic shafts and one example made an axosomatic synapse; in area 3 97% made synapses on to dendritic spines and 3% contacted dendritic shafts. A number of the spines receiving synapses from degenerating commissural axon terminals were traced to their parent dendrites and these were of the pyramidal type. The cell soma and the majority of the dendritic shafts receiving synapses from commissural terminals were of the large stellate type although some of the dendritic shafts were probably those of small stellate cells. In the motor cortex degenerating commissural axon terminals were found in all cortical layers but were relatively more dense in layer I, the upper part of layer III, the upper part of layer V and the lowest part of layer V with layer V I; in the somatic sensory cortex most degenerating commissural terminals were found in the superficial half of the cortex. Following lesions of the primary somatic sensory cortex (SI) or of area 6 of the premotor cortex, degenerating terminals making asymmetric synapses were found in the motor cortex. Of the terminals of association fibres from SI, 82% made synapses on to dendritic spines and 18% on to dendritic shafts; of those fibres from area 6, 76% made synapses on to dendritic spines and 24% on to dendritic shafts. For both these association fibre connections, a proportion of the dendritic shafts contacted were clearly identifiable as those of large stellate cells. Terminals of both association connections occurred in all cortical layers with no obvious concentrations at any particular depth.


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