Fine structure of dendrites in the superficial neocortical neuropil

doi:10.1016/0014-4886(61)90049-8

Experimental Neurology

Volume 4, Issue 6, December 1961, Pages 507-530

https://doi.org/10.1016/0014-4886(61)90049-8 Get rights and content

Abstract

Electron microscope observations have been made on neuron cell bodies, axosomatic and axodendritic synapses, and dendrites in the superficial (0.4–0.5 mm) neocortex of adult cat middle suprasylvian gyrus. Particular attention is focused on the fine structure of dendrites in this region of neocortex. The overt characteristics of neuron cell bodies are similar to those described by others. The present study emphasizes the presence of granular inclusion bodies and regions of apparent membrane thickenings in the cytoplasm. The latter are attributable to lamination of cisternal membranes of the endoplasmic reticulum. Dendrites in the superficial neuropil contain characteristic tubules and mitochondria which may occasionally be of extraordinary length (over 9 μ). Multivesicular bodies are found in relatively large numbers of dendrites, often intimately associated with synaptic complexes. Sectors of the limiting membrane of these bodies exhibit thickenings similar to those found at postsynaptic axodendritic sites. Numerous axosomatic synapses on dendritic spines are observed, but the spine apparatus described by Gray has rarely been encountered. Processes as small as 0.03 μ in diameter are found in continuity with larger dendritic elements containing tubules and multivesicular bodies. These processes, with characteristic tubules cut transversely, are found interposed between virtually all elements of the neuropil, sometimes in synaptic relation with axonal terminals. Criteria for identifying them as dendritic terminals are presented and the role of these processes in the functional activity of the neuropil is briefly discussed.

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Dendritic spinules are thin protrusions, formed by neuronal spines, not adequately resolved by diffraction-limited light microscopy, which has limited our understanding of their behavior. Here we performed rapid structured illumination microscopy and enhanced resolution confocal microscopy to study spatiotemporal spinule dynamics in cortical pyramidal neurons. Spinules recurred at the same locations on mushroom spine heads. Most were short-lived, dynamic, exploratory, and originated near simple PSDs, whereas a subset was long-lived, elongated, and associated with complex PSDs. These subtypes were differentially regulated by Ca²⁺ transients. Furthermore, the postsynaptic Rac1-GEF kalirin-7 regulated spinule formation, elongation, and recurrence. Long-lived spinules often contained PSD fragments, contacted distal presynaptic terminals, and formed secondary synapses. NMDAR activation increased spinule number, length, and contact with distal presynaptic elements. Spinule subsets, dynamics, and recurrence were validated in cortical neurons of acute brain slices. Thus, we identified unique properties, regulatory mechanisms, and functions of spinule subtypes, supporting roles in neuronal connectivity.
Multivesicular bodies in neurons: Distribution, protein content, and trafficking functions
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Citation Excerpt :
MVBs have only rarely been documented in normal CNS axons under physiological conditions (Janetzko et al., 1989; Roizin et al., 1967; Vitalis et al., 2008). Some investigators concluded that MVBs may not exist there at all (Castel et al., 1992; Hirano and Llena, 1995; Pappas and Purpura, 1961). Based on the apparent lack of MVBs in CNS axons, Pappas and Purpura (1961) suggested that MVBs may aid in the ultrastructural distinction between dendritic and axonal processes.
Multivesicular bodies (MVBs) are intracellular endosomal organelles characterized by multiple internal vesicles that are enclosed within a single outer membrane. MVBs were initially regarded as purely prelysosomal structures along the degradative endosomal pathway of internalized proteins. MVBs are now known to be involved in numerous endocytic and trafficking functions, including protein sorting, recycling, transport, storage, and release. This review of neuronal MVBs summarizes their research history, morphology, distribution, accumulation of cargo and constitutive proteins, transport, and theories of functions of MVBs in neurons and glia. Due to their complex morphologies, neurons have expanded trafficking and signaling needs, beyond those of “geometrically simpler” cells, but it is not known whether neuronal MVBs perform additional transport and signaling functions. This review examines the concept of compartment-specific MVB functions in endosomal protein trafficking and signaling within synapses, axons, dendrites and cell bodies. We critically evaluate reports of the accumulation of neuronal MVBs based on evidence of stress-induced MVB formation. Furthermore, we discuss potential functions of neuronal and glial MVBs in development, in dystrophic neuritic syndromes, injury, disease, and aging. MVBs may play a role in Alzheimer's, Huntington's, and Niemann–Pick diseases, some types of frontotemporal dementia, prion and virus trafficking, as well as in adaptive responses of neurons to trauma and toxin or drug exposure. Functions of MVBs in neurons have been much neglected, and major gaps in knowledge currently exist. Developing truly MVB-specific markers would help to elucidate the roles of neuronal MVBs in intra- and intercellular signaling of normal and diseased neurons.
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1992, Electron Microscopy Reviews
The present work attempts to demonstrate that cryofixation is a valuable method for the study of the nervous tissue. The use of the newly developed methods of cryofixation and freeze-etching without fixatives or cryoprotectants allows new exciting perspectives for the electron microscopical observation of cellular components, emphasizing their three-dimensional morphological structures. Significant contributions have been made on the fine structure of the cytoskeleton, cell membranes and cell organelles. The components of the cytoskeleton are distributed in different composition through the perikarya, dendrites and axon. The ubiquitous presence of the cytoskeleton suggests a crucial role in the functional activities of the neurons, especially in relation to the intracellular communication and to developmental and regeneration processes. Vitrified cellular membranes of myelin sheaths and rod outer segments have been observed in hydrated state by using cryofixation and cryotransfer techniques. These procedures allow new insights into the supramolecular structure and an approximation of morphological data to the present biophysical membrane model including a critical comparison with the current descriptions gained by conventional electron microscopy.
Ultrastructure of synapses and golgi analysis of neurons in neocortex of the lateral gyrus (visual cortex) of the dolphin and pilot whale
1990, Brain Research Bulletin
Qualitative and computerized quantitative analyses of ultrastructural features of synapses in different layers of the primary visual cortex in the dolphin (Stenella coeruleoalba) and the pilot whale (Globicephala melaena) were carried out. Also, Golgi and cytoarchitectonic analyses were performed in the same species of cetaceans and, additionally, in Tursiops truncatus and Phocaena phocaena. It was found that on a synaptic level, as well as in cytoarchitectonic and Golgi features, the neocortex of cetaceans combines evolutionary progressive features and conservative features with a marked prevalence of the latter. Thus, the total number of synapses in visual neocortex in cetaceans is closer to this value in higher Primates. On the other hand, the laminar density of synapses per mm³ is generally the same in all layers in cetacean visual cortex and numerically is close to values found in small lissencephalic brains. Also, the synapse/neuron ratio in the dolphin visual cortex is of the same order as in cortices of rodents and lagomorphs and much higher than in cortices of advanced terrestrial mammals. Layers I and II contain approximately 70% of the total synapses in the cortical slab through visual cortex. Layer I also contains the extraverted dendrites of neurons of layer II and thus these two layers resemble a paleoarchicortical type of organization superimposed on a more typical neocortical organization of the lower cortical layers. In this respect the convexity neocortex of cetaceans is generally similar to the neocortices of phylogenetically ancient extant mammals such as basal Insectivora and Chiroptera.
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1980, Neuroscience Letters
Neuropil from a number of sites in both mammalian and inframammalian species was examined by electron microscopy. Complex micropinocytotic invaginations in which a tongue of cytoplasm extended into the endocytotic indentation of the cell membrane, were observed in all tissues. These complex membrane infoldings occurred at both chemical and electrotonic synapses. Coated invaginations of apposed membranes, at which infoldings occurred directly opposite each other, were also observed at the interfaces between neighboring dendrites. These observations indicate that micropinocytotic membrane infoldings involving the coordinated activity of adjacent neuronal membranes occur in a wide variety of tissues. Coordinated exocytosis/endocytosis may provide a mechanism for interneuronal bulk transport of material, both at synapses and at non-synaptic sites, in the central nervous system.
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1978, Brain Research
Newborn (P-0 and P-1) through 6-day-old (P-6) rats were studied using light microscopic (Golgi) and ultrastructural methods. Previous studies demonstrated that early-formed synapses are concentrated at specific cortical depths, i.e. in strata. The present study shows that the synaptic stratum in the marginal zone corresponds to a dense fiber plexus and few somata (Cajal-Retzius cells). Axons in this zone almost exclusively form synapses on distal branches of dendrites originating in deeper lamina. In newborn neocortex there is a second synaptic stratum located deep to the cortical plate. It contains numerous axosomatic and axoproximal dendritic synapses as well as the most highly differentiated somata and proximal dendrites. By age P-6 there are 3 synaptic strata; one each in the marginal zone, cortical plate and ‘subplate’ layers. For all 3 strata a neuron's most differentiated dendrites are directed towards, traverse or run within, the nearest synaptic stratum. We conclude that, throughout the first postnatal week, the most mature dendrites of a given neuron generally occur at depths where synapse density is highest. At P-0 the most mature somata are similarly related to synaptic density.

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¹: Supported in part by grants from the National Institutes of Health (B-2314 C₁ and B-1312 C₄) and the United Cerebral Palsy Foundation. Dr. Purpura is a Senior Research Fellow, National Institute of Neurological Diseases and Blindness. Various aspects of this study were presented in part elsewhere (17).

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Fine structure of dendrites in the superficial neocortical neuropil

Abstract

Intern. Rev. Neurobiol

Electron microscopy of the cerebral cortex. I. Ultrastructure and histochemistry of synaptic junctions

Bull. Johns Hopkins Hosp.

Submicroscopic morphology and function of the synapse

Exptl. Cell. Research Suppl.

The properties of dendrites

An electron microscope study of regenerating nerve fibers

Z. Zellforsch. u. mikroskop. Anat.

Electron microscopy of neuroglial fibers of the cerebral cortex

J. Biophys. Biochem. Cytol.

Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study

J. Anat.

Ultrastructure of synapses of the cerebral cortex and of certain specialisations of neuroglial membranes

Synaptic and ephaptic transmission

Handbook Physiol., Sect. 1, Neurophysiol.

Die Feinstruktur des molecularen Rindengraues und ihre physiologische Bedeutung

Z. Zellforsch. u. mikroskop. Anat.

Postnatal ontogenesis of cat neocortex

J. Comp. Neurol.