The Cochlear Nucleus: Neuronal Types and Their Synaptic Organization

The auditory system, like other sensory systems, comprises multiple neuronal pathways, each conveying information from the periphery to the forebrain via distinct sets of neurons and each with its own role to play in the function of the system. In the cochlear nuclear complex, the part of the brain that receives inputs from the cochlea via the eighth nerve, the neurons that participate in the separate pathways are, to a large extent, distinguishable from one another morphologically and many are also segregated spatially, making them especially accessible for detailed study. The results of detailed anatomical studies of the different cell types provide a framework for relating and interpreting the results of studies of the physiology, connectivity and transmitter neurochemistry of the different pathways.

[1]  D. Trune,et al.  Influence of neonatal cochlear removal on the development of mouse cochlear nucleus: II. Dendritic morphometry of its neurons , 1982, The Journal of comparative neurology.

[2]  J. Moore,et al.  The primate cochlear nuclei: loss of lamination as a phylogenetic process. , 1980, The Journal of comparative neurology.

[3]  A S Feng,et al.  Functional organization of the cochlear nucleus of rufous horseshoe bats (Rhinolophus rouxi): Frequencies and internal connections are arranged in slabs , 1985, The Journal of comparative neurology.

[4]  D. K. Morest,et al.  The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Electron microscopy , 1982, Neuroscience.

[5]  J. Conlee,et al.  Descending inputs to the caudal cochlear nucleus of the cat: Degeneration and autoradiographic studies , 1979, The Journal of comparative neurology.

[6]  K K Osen,et al.  Stellate neurons in rat dorsal cochlear nucleus studied with combined Golgi impregnation and electron microscopy: synaptic connections and mutual coupling by gap junctions , 1984, Journal of neurocytology.

[7]  H. Tokuno,et al.  Auditory brainstem in the mole (Mogera): Nuclear configurations and the projections to the inferior colliculus , 1990, The Journal of comparative neurology.

[8]  Takeshi Kubo,et al.  Distribution and fine structure of neuronal elements containing glutamate decar☐ylase in the rat cochlear nucleus , 1985, Brain Research.

[9]  N. Cant,et al.  Axons from non-cochlear sources in the anteroventral cochlear nucleus of the cat. A study with the rapid golgi method , 1978, Neuroscience.

[10]  R W Rodieck,et al.  Retinal ganglion cells: properties, types, genera, pathways and trans-species comparisons. , 1983, Brain, behavior and evolution.

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

[12]  R. Roberts,et al.  GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil , 1987, The Journal of comparative neurology.

[13]  K K Osen,et al.  The cochlear nuclei in man. , 1979, The American journal of anatomy.

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

[15]  D. Yurgelun-Todd,et al.  The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Horseradish peroxidase labelling of identified cell types , 1982, Neuroscience.

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

[17]  R. Wickesberg,et al.  Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  R. Irving,et al.  The organization of the posterior ventral cochlear nucleus in the rat , 1966, The Journal of comparative neurology.

[19]  J. H. Casseday,et al.  Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei , 1986, The Journal of comparative neurology.

[20]  L. Schweitzer,et al.  Development of oriented dendritic fields in the dorsal cochlear nucleus of the hamster , 1985, Neuroscience.

[21]  Michael R. Martin Morphology of the cochlear nucleus of the normal and reeler mutant mouse , 1981, The Journal of comparative neurology.

[22]  M. Feldman,et al.  Anatomical aspects of the cochlear nucleus and superior olivary complex. , 1970, Contributions to sensory physiology.

[23]  R. Wenthold,et al.  Evidence for a glycinergic pathway connecting the two cochlear nuclei: an immunocytochemical and retrograde transport study , 1987, Brain Research.

[24]  G. R. Farley,et al.  Descending projections from the superior olivary complex to the cochlear nucleus of the cat , 1987, The Journal of comparative neurology.

[25]  W. Warr,et al.  A study of the cochlear nuclei and ascending auditory pathways of the medulla , 1962, The Journal of comparative neurology.

[26]  K K Osen,et al.  Cytoarchitecture of the cochlear nuclei in the cat , 1969 .

[27]  J. Zook,et al.  Origin of ascending projections to inferior colliculus in the mustache bat, Pteronotus parnellii , 1982, The Journal of comparative neurology.

[28]  J. Zook,et al.  Connections and frequency representation in the auditory brainstem of the mustache bat, Pteronotus parnellii , 1989, The Journal of comparative neurology.

[29]  E. Rouiller,et al.  The central projections of intracellularly labeled auditory nerve fibers in cats: an analysis of terminal morphology. , 1986, The Journal of comparative neurology.

[30]  J. Conlee,et al.  Descending projections from the inferior colliculus to the dorsal cochlear nucleus in the cat: An autoradiographic study , 1982, Neuroscience.

[31]  K. Osen Course and termination of the primary afferents in the cochlear nuclei of the cat. An experimental anatomical study. , 1970, Archives italiennes de biologie.

[32]  Professor Dr. George D. Pollak,et al.  The Neural Basis of Echolocation in Bats , 1989, Zoophysiology.

[33]  E. S. Kane Descending projections to specific regions of cat cochlear nucleus: A light microscopic study , 1976, Experimental Neurology.

[34]  K. Osen,et al.  GABA-like and glycine-like immunoreactivities of the cochlear root nucleus in rat , 1991, Journal of neurocytology.

[35]  R. Wenthold,et al.  Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor , 1986, Brain Research.

[36]  R. Romand,et al.  Survey of intracellular recording in the cochlear nucleus of the cat , 1978, Brain Research.

[37]  E. Rouiller,et al.  Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat , 1984, The Journal of comparative neurology.

[38]  C. Sotelo,et al.  Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultra-structural study. , 1973, Brain research.

[39]  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.

[40]  D. Trune,et al.  Influence of neonatal cochlear removal on the development of mouse cochlear nucleus: I. Number, size, and density of its neurons , 1982, The Journal of comparative neurology.

[41]  D. Ryugo,et al.  Endbulbs of held and spherical bushy cells in cats: Morphological correlates with physiological properties , 1989, The Journal of comparative neurology.

[42]  N. Cant,et al.  Pathways connecting the right and left cochlear nuclei , 1982, The Journal of comparative neurology.

[43]  R. Irving,et al.  Second Order Neurons in the Acoustic Nerve , 1962, Science.

[44]  S. Potashner Uptake and Release of D‐Aspartate in the Guinea Pig Cochlear Nucleus , 1983, Journal of neurochemistry.

[45]  Ramón y Cajal,et al.  Histologie du système nerveux de l'homme & des vertébrés , 1909 .

[46]  K. A. Hutson,et al.  Cytoarchitectonic atlas of the cochlear nucleus of the chinchilla, Chinchilla laniger , 1990, The Journal of comparative neurology.

[47]  J. M. Harrison,et al.  The anterior ventral cochlear nucleus , 1965, The Journal of comparative neurology.

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

[49]  H. Schweizer The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum) , 1981, The Journal of comparative neurology.

[50]  J. Noort The structure and connections of the inferior colliculus : an investigation of the lower auditory system , 1969 .

[51]  N. Strominger,et al.  Ascending brain stem projections of the anteroventral cochlear nucleus in the rhesus monkey , 1971, The Journal of comparative neurology.

[52]  M. Merchán,et al.  Morphology of cochlear root neurons in the rat , 1988, Journal of neurocytology.

[53]  S. Chamberlain Neuroanatomical aspects of the gerbil inner ear: Light microscope observations , 1977, The Journal of comparative neurology.

[54]  N. Kiang,et al.  Single unit activity in the posteroventral cochlear nucleus of the cat , 1975, The Journal of comparative neurology.

[55]  M. Liberman,et al.  Auditory-nerve response from cats raised in a low-noise chamber. , 1978, The Journal of the Acoustical Society of America.

[56]  N. Cant Identification of cell types in the anteroventral cochlear nucleus that project to the inferior colliculus , 1982, Neuroscience Letters.

[57]  D. A. Godfrey,et al.  Quantitative histochemical mapping of enzymes of the cholinergic system in cat cochlear nucleus. , 1977, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[58]  Michael R. Martin Acetylcholinesterase‐positive fibers and cell bodies in the cochlear nuclei of normal and reeler mutant mice , 1981, The Journal of comparative neurology.

[59]  Donata Oertel,et al.  Tonotopic projection from the dorsal to the anteroventral cochlear nucleus of mice , 1988, The Journal of comparative neurology.

[60]  H. Killackey,et al.  Ascending auditory projections to the inferior colliculus in the adult gerbil, Meriones unguiculatus , 1983, The Journal of comparative neurology.

[61]  E. S. Kane,et al.  Neuronal types in the deep dorsal cochlear nucleus of the cat: I. Giant neurons , 1981, The Journal of comparative neurology.

[62]  G. L. Rasmussen,et al.  Ultrastructural characteristics of synaptic endings in the cochlear nucleus having acetylcholinesterase activity. , 1971, Brain research.

[63]  W. S. Rhode,et al.  Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus , 1989, The Journal of comparative neurology.

[64]  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.

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

[66]  K. Osen,et al.  The Human Cochlear Nuclei , 1979 .

[67]  R. Snyder,et al.  Intrinsic connections within and between cochlear nucleus subdivisions in cat , 1988, The Journal of comparative neurology.

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

[69]  D. Oertel,et al.  Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice , 1989, The Journal of comparative neurology.

[70]  W. R. Webster,et al.  Neuronal organization of the rabbit cochlear nucleus: Some anatomical and electrophysiological observations , 1981, The Journal of comparative neurology.

[71]  D. A. Godfrey,et al.  Distribution of gamma-aminobutyric acid, glycine, glutamate and aspartate in the cochlear nucleus of the rat. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[72]  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.

[73]  Joe C. Adams,et al.  Patterns of glutamate decarboxylase immunostaining in the feline cochlear nuclear complex studied with silver enhancement and electron microscopy , 1987, The Journal of comparative neurology.

[74]  J. Willott The Auditory psychobiology of the mouse , 1983 .

[75]  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.

[76]  J. Zempel,et al.  Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig , 1986, Brain Research.

[77]  N. Strominger,et al.  The cytoarchitecture of the human anteroventral cochlear nucleus , 1973, The Journal of comparative neurology.

[78]  R. Snyder,et al.  Topographic organization of the central projections of the spiral ganglion in cats , 1989, The Journal of comparative neurology.

[79]  W. S. Rhode,et al.  Electron microscopic features of physiologically characterized, HRP‐labeled fusiform cells in the cat dorsal cochlear nucleus , 1985, The Journal of comparative neurology.

[80]  R. L. Marie,et al.  Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus , 1991, Hearing Research.

[81]  W. S. Rhode,et al.  Characterization of HRP‐labeled globular bushy cells in the cat anteroventral cochlear nucleus , 1987, The Journal of comparative neurology.

[82]  D. Oliver,et al.  Dorsal cochlear nucleus projections to the inferior colliculus in the cat: A light and electron microscopic study , 1984, The Journal of comparative neurology.

[83]  N. Cant,et al.  The fine structure of two types of stellate cells in the anterior division of the anteroventral cochlear nucleus of the cat , 1981, Neuroscience.

[84]  K. Osen,et al.  Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. , 1984, Archives italiennes de biologie.

[85]  N. Cant Projections to the lateral and medial superior olivary nuclei from the spherical and globular bushy cells of the anteroventral cochlear nucleus , 1991 .

[86]  E. Mugnaini GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: Light and electron microscopic immunocytochemistry , 1985, The Journal of comparative neurology.

[87]  T. E. Benson,et al.  Synapses formed by olivocochlear axon branches in the mouse cochlear nucleus , 1990, The Journal of comparative neurology.

[88]  W. Warr Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat. , 1966, Experimental neurology.

[89]  Nell B. Cant,et al.  The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope , 1979, Neuroscience.

[90]  W. D. Neff Contributions to sensory physiology , 1965 .

[91]  Charles I. Berlin,et al.  Hearing science : recent advances , 1985 .

[92]  R. Wenthold,et al.  Ultrastructural localization of GABA-immunoreactive terminals in the anteroventral cochlear nucleus of the guinea pig , 1988, Hearing Research.

[93]  W. Pirsig,et al.  Differentiation of nerve endings in the cochlear nucleus on morphological and experimental basis. , 1979, Acta oto-laryngologica.

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

[95]  K. Osen,et al.  Histochemical localization of cholinesterases in the cochlear nuclei of the cat, with notes on the origin of acetylcholinesterase-positive afferents and the superior olive. , 1969, Brain research.

[96]  R. Wenthold,et al.  Glycine receptor immunoreactivity in the ventral cochlear nucleus of the guinea pig , 1988, The Journal of comparative neurology.

[97]  L. F. Kromer,et al.  Cochlear nucleus innervation by central norepinephrine neurons in the rat , 1976, Brain Research.

[98]  D. K. Morest,et al.  Relations between auditory nerve endings and cell types in the cat's anteroventral cochlear nucleus seen with the Golgi method and nomarski optics , 1975, The Journal of comparative neurology.

[99]  Vestibular Systems,et al.  Neural mechanisms of the auditory and vestibular systems , 1960 .

[100]  K. Osen,et al.  The cochlear nuclei in the common porpoise, Phocaena phocaena , 1965, The Journal of comparative neurology.

[101]  J. A. Hirsch,et al.  Synaptic connections in the dorsal cochlear nucleus of mice, in vitro. , 1988, The Journal of physiology.

[102]  E. Rouiller,et al.  The central projections of intracellularly labeled auditory nerve fibers in cats , 1984, The Journal of comparative neurology.

[103]  Josef Syka,et al.  Neuronal Mechanisms of Hearing , 1981, Springer US.

[104]  D. Oertel,et al.  Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[105]  L. Schweitzer,et al.  Differentiation of the giant and fusiform cells in the dorsal cochlear nucleus of the hamster. , 1985, Brain research.

[106]  Joe C. Adams,et al.  Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts , 1976, The Journal of comparative neurology.

[107]  I. Schwartz The differential distribution of label following uptake of 3H-labeled amino acids in the dorsal cochlear nucleus of the cat An autoradiographic study , 1981, Experimental Neurology.

[108]  R. Irving,et al.  Ascending connections of the anterior ventral cochlear nucleus in the rat , 1966, The Journal of comparative neurology.

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

[110]  J. Zook,et al.  Cytoarchitecture of auditory system in lower brainstem of the mustache bat, Pteronotus parnellii , 1982, The Journal of comparative neurology.

[111]  Richard P. Bobbin,et al.  Neurobiology of hearing : the cochlea , 1986 .

[112]  T. Reese,et al.  The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus. , 1966, The American journal of anatomy.

[113]  D. Webster Projection of the cochlea to cochlear nuclei in merriam's kangaroo rat , 1971, The Journal of comparative neurology.

[114]  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.

[115]  D. Rl Some unresolved problems concerning the cochlear nerve. , 1976 .

[116]  N. Cant,et al.  Organization of the neurons in the anterior division of the anteroventral cochlear nucleus of the cat. Light-microscopic observations , 1979, Neuroscience.

[117]  J. R. Hughes,et al.  Microelectrode studies of the cochlear nuclei of the cat. , 1959, Bulletin of the Johns Hopkins Hospital.

[118]  D. A. Godfrey,et al.  Quantitative histochemical mapping of candidate transmitter amino acids in cat cochlear nucleus. , 1977, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[119]  C. G. Benson,et al.  Retrograde transport of [3H]glycine from the cochlear nucleus to the superior olive in the guinea pig , 1990, The Journal of comparative neurology.

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

[121]  K. Osen,et al.  The cochlear nerve in the cat: Topography, cochleotopy, and fiber spectrum , 1978, The Journal of comparative neurology.

[122]  E. C. Kane,et al.  Octopus cells in the cochlear nucleus of the cat: heterotypic synapses upon homeotypic neurons. , 1973, The International journal of neuroscience.

[123]  A. B. Graham Sensorineural hearing processes and disorders , 1967 .

[124]  Jean K. Moore,et al.  Glutamic acid decarboxylase‐like immunoreactivity in brainstem auditory nuclei of the rat , 1987, The Journal of comparative neurology.

[125]  E. S. Kane Descending inputs to octopus cell area of the cat cochlear nucleus: An electron microscopic study , 1977, The Journal of comparative neurology.

[126]  E. Rouiller,et al.  Central projections of intracellularly labeled auditory nerve fibers in cats: Morphometric correlations with physiological properties , 1988, The Journal of comparative neurology.

[127]  C. Hackney,et al.  The distribution of spherical cells in the anteroventral cochlear nucleus of the guinea pig. , 1986, British journal of audiology.

[128]  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.

[129]  E. S. Kane Descending inputs to the cat dorsal cochlear nucleus: An electron microscopic study , 1977, Journal of neurocytology.

[130]  D. Ryugo,et al.  The dorsal cochlear nucleus of the mouse: A light microscopic analysis of neurons that project to the inferior colliculus , 1985, The Journal of comparative neurology.

[131]  R. L. Marie,et al.  The form and distribution of GABAergic synapses on the principal cell types of the ventral cochlear nucleus of the cat , 1989, Hearing Research.

[132]  R. Wenthold,et al.  Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex , 1987, Neuroscience.

[133]  D. K. Morest,et al.  The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Golgi and Nissl methods , 1982, Neuroscience.

[134]  Joe C. Adams Multipolar cells in the ventral cochlear nucleus project to the dorsal cochlear nucleus and the inferior colliculus , 1983, Neuroscience Letters.

[135]  J. H. Casseday,et al.  Projections to laminae in dorsal cochlear nucleus in the tree shrew, Tupaia glis , 1979, Brain Research.

[136]  M. C. Brown,et al.  Brainstem branches from olivocochlear axons in cats and rodents , 1988, The Journal of comparative neurology.

[137]  E. S. Kane,et al.  Development of the octopus cell area in the cat ventral cochlear nucleus. , 1977, The American journal of anatomy.

[138]  E. Ostapoff,et al.  Uptake and retrograde transport of [3H]GABA from the cochlear nucleus to the superior olive in the guinea pig. , 1990, Journal of chemical neuroanatomy.

[139]  D. Oertel,et al.  Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[140]  J. Adams Neuronal morphology in the human cochlear nucleus. , 1986, Archives of otolaryngology--head & neck surgery.

[141]  P. Manis,et al.  Responses to parallel fiber stimulation in the guinea pig dorsal cochlear nucleus in vitro. , 1989, Journal of neurophysiology.

[142]  N. Kiang,et al.  Central trajectories of type II spiral ganglion neurons , 1988, The Journal of comparative neurology.

[143]  M M Merzenich,et al.  Anatomical and physiological evidence for auditory specialization in the mountain beaver (Aplodontia rufa). , 1973, Brain research.

[144]  Y. Ibata,et al.  The fine structure of synapses in relation to the large spherical neurons in the anterior ventral cochlear of the cat , 1976, Journal of neurocytology.

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

[146]  R. Gulley,et al.  Non-primary afferents to the principal cells of the rostral anteroventral cochlear nucleus of the guinea pig. , 1978, The American journal of anatomy.

[147]  Terrance Raymond Bourk,et al.  Electrical responses of neural units in the anteroventral cochlear nucleus of the cat , 1976 .

[148]  B. Norris,et al.  Tonotopic organization of the anteroventral cochlear nucleus of the cat , 1981, Hearing Research.