Stellate neurons in rat dorsal cochlear nucleus studied with combined Golgi impregnation and electron microscopy: synaptic connections and mutual coupling by gap junctions

SummaryStellate neurons in the outer two layers of the rat dorsal cochlear nucleus (DCN) were studied by the Golgi-EM method. Stellate cell bodies are usually spherical or ovoidal and range from 9 μm to 14 μm in mean diameter. The smallest cells are situated underneath the ependymal layer and the largest cells in layer 2. Primary dendrites are short, thin and smooth and arise abruptly from the perikaryon, without a tapering main stem. Meandering secondary and tertiary dendrites extend in all directions, carry few pleomorphic spines lacking a spine apparatus and often show artifactual beading. The axons are impregnated only for a short distance (10–45 μm). The nucleus is indented, the nucleolus varies in position, and the chromatin, evenly dispersed in the centre, forms small clumps along the nuclear envelope. The cytoplasm is rich in free polyribosomes and contains scattered cisterns of granular endoplasmic reticulum. Varicosities of thin fibres, containing round synaptic vesicles, form asymmetric synapses on perikarya, dendritic shafts and spines of stellate cells. Such fibres run parallel to the long axis of the DCN or are oriented radially and are interpreted as axons of cochlear granule cells. Two kinds of bouton containing pleomorphic vesicles, one kind electron lucent and the other electron dense, form symmetric synapses on perikarya and dendritic shafts of stellate cells. The lucent boutons occur more frequently than the dense boutons, especially on the distal dendritic branches. The boutons with pleomorphic vesicles presumably represent terminals of local circuit neurons, probably the stellate and cartwheel cells.In addition, stellate cells show numerous dendro-somatic and dendro-dendritic appositions characterized by gap junctions and puncta adhaerentia. Most of the dendrites involved in these appositions resemble stellate cell dendrites and it is concluded that DCN stellate cells are coupled electrotonically with one another. The axons of stellate cells acquire a thin myelin sheath. Since the Golgi impregnation did not stain axons of stellate cells past this point, we were unable to demonstrate the synaptic targets of stellate cells.

[1]  Enrico Mugnaini,et al.  Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse , 1980, The Journal of comparative neurology.

[2]  W. J. Hamilton,et al.  The localization of sodium and calcium to Schwann cell paranodal loops at nodes of Ranvier and of calcium to compact myelin , 1980, Journal of neurocytology.

[3]  A. Peters,et al.  A new procedure for examining Golgi impregnated neurons by light and electron microscopy , 1977, Journal of neurocytology.

[4]  E. Mugnaini,et al.  Electron Microscopy: Preparation of Neural Tissues for Electron Microscopy , 1981 .

[5]  E C Kane,et al.  Synaptic organization in the dorsal cochlear nucleus of the cat: A light and electron microscopic study , 1974 .

[6]  V. Tennyson The Fine Structure of the Nervous System. , 1970 .

[7]  E C Kane,et al.  Patterns of degeneration in the caudal cochlear nucleus of the cat after cochlear ablation , 1974, The Anatomical record.

[8]  R. L. Nó,et al.  Anatomy of the eighth nerve: III.—General plan of structure of the primary cochlear nuclei , 1933 .

[9]  Enrico Mugnaini,et al.  Neuronal Circuits in the Dorsal Cochlear Nucleus , 1981 .

[10]  S. Palay,et al.  Cerebellar Cortex: Cytology and Organization , 1974 .

[11]  E. T. Pierce Histogenesis of the dorsal and ventral cochlear nuclei in the mouse. An autoradiographic study , 1967, The Journal of comparative neurology.

[12]  Professor Dr. John C. Eccles,et al.  The Cerebellum as a Neuronal Machine , 1967, Springer Berlin Heidelberg.

[13]  J. DeFelipe,et al.  The Golgi-EM procedure: a tool to study neocortical interneurons. , 1981, Progress in clinical and biological research.

[14]  T. Blackstad,et al.  Pyramidal neurones of the dorsal cochlear nucleus: A golgi and computer reconstruction study in cat , 1984, Neuroscience.

[15]  T. Powell,et al.  Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[16]  J. Sloper,et al.  Gap junctions between dendrites in the primate neocortex. , 1972, Brain research.

[17]  Adams Jc A fast, reliable silver-chromate Golgi method for perfusion-fixed tissue. , 1979 .

[18]  A. Peters,et al.  Synaptic relationships between a multipolar stellate cell and a pyramidal neuron in the rat visual cortex. A combined Golgi-electron microscope study , 1980, Journal of neurocytology.

[19]  D. K. Morest,et al.  The neuronal architecture of the cochlear nucleus of the cat , 1974, The Journal of comparative neurology.

[20]  Gray Eg Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study , 1959 .

[21]  C. Sotelo,et al.  Gap junctions in ventral cochlear nucleus of the rat. A possible new example of electrotonic junctions in the mammalian C.N.S. , 1976, Neuroscience.

[22]  Raphael Lorente De No,et al.  The Primary Acoustic Nuclei , 1981 .

[23]  J. Jansen,et al.  The Comparative Anatomy and Histology of the Cerebellum: The Human Cerebellum, Cerebellar Connections, and Cerebellar Cortex , 1972 .

[24]  K K Osen,et al.  Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse , 1980, Journal of neurocytology.

[25]  D. Webster,et al.  Cochlear nuclear complex of mice. , 1982, The American journal of anatomy.

[26]  E. Mugnaini,et al.  Cartwheel neurons of the dorsal cochlear nucleus: A Golgi‐electron microscopic study in rat , 1984, The Journal of comparative neurology.

[27]  A. Peters Morphological correlates of epilepsy: cells in the cerebral cortex. , 1980, Advances in neurology.

[28]  J. Disterhoft,et al.  Neuronal morphology of the rabbit cochlear nucleus , 1980, The Journal of comparative neurology.

[29]  J. Altman,et al.  Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incoorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions , 1966, The Journal of comparative neurology.

[30]  E. Mugnaini,et al.  Subsurface and cytoplasmic cisterns associated with mitochondria in pyramidal neurons of the rat dorsal cochlear nucleus , 1981, Neuroscience.

[31]  D. Oliver,et al.  Selective labeling of spiral ganglion and granule cells with D- aspartate in the auditory system of cat and guinea pig , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  J. Altman,et al.  Development of the brain stem in the rat. III. Thymidine‐radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla , 1980, The Journal of comparative neurology.

[33]  E. S. Kane,et al.  Desending and intrinsic inputs to dorsal cochlear nucleus of cats: A horseradish peroxidase study , 1977, Neuroscience.

[34]  F. Wouterlood,et al.  Chemical reduction of silver chromate: a procedure for electron microscopical analysis of Golgi-impregnated neurons , 1983, Journal of Neuroscience Methods.

[35]  R. Llinás,et al.  SPECIALIZED MEMBRANE JUNCTIONS BETWEEN NEURONS IN THE VERTEBRATE CEREBELLAR CORTEX , 1972, The Journal of cell biology.

[36]  F. Sharp,et al.  Autoradiographic maps of regional brain glucose consumption in resting, awake rats using [14c] 2‐deoxyglucose , 1978, The Journal of comparative neurology.

[37]  C. Ribak,et al.  Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase , 1978, Journal of neurocytology.

[38]  T. Powell,et al.  Dendro-dendritic and reciprocal synapses in the primate motor cortex , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[39]  E. Raviola,et al.  Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits , 1975, The Journal of cell biology.

[40]  F. Wouterlood Light microscopic identification and photography of Golgi impregnated central nervous system neurons during sectioning for electron microscopy. , 1979, Stain technology.

[41]  N. Lemkey-Johnston,et al.  Types and distribution of synapses upon basket and stellate cells of the mouse cerebellum: An electron microscopic study , 1968, The Journal of comparative neurology.

[42]  M. Colonnier Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[43]  R. H. Browner,et al.  The cytoarchitecture of the dorsal cochlear nucleus in the 3‐month‐ and 26‐month‐old C57BL/6 mouse: A golgi impregnation study , 1982, The Journal of comparative neurology.

[44]  P. Rakić Extrinsic cytological determinants of basket and stellate cell dendritic pattern in the cerebellar molecular layer , 1972, The Journal of comparative neurology.

[45]  W. S. Rhode,et al.  Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus , 1983, The Journal of comparative neurology.