A physiological and structural study of neuron types in the cochlear nucleus. II. Neuron types and their structural correlation with response properties

The present study examined the morphological cell types of neurons labeled with intracellular horseradish peroxidase injections, many of them following electrophysiological recordings in the cochlear nucleus of gerbils and chinchillas. Most of the subdivisions and neuronal types previously described in the cat were identified in the present material, including spherical and globular bushy cells, stellate, bushy multipolar, elongate, octopus, and giant cells in the ventral cochlear nucleus, and a cartwheel cell in the dorsal cochlear nucleus. In many cases these structurally distinct neurons were correlated with their characteristic responses to stimulation by sound or intracellular injection of depolarizing current. The dendritic terminals of the elongate, antenniform, and clavate cells of the posteroventral cochlear nucleus link each of these cell types with neighboring structures in distinct patterns, which may provide a basis for differences in synaptic organization. These cell types differ from each other and from the stellate cells of the anteroventral cochlear nucleus. Despite their heterogeneous morphology, most of these neurons had a regular discharge in response to stimulation (choppers). Irregularly firing neurons (primary‐like) had very different structures, e. g., the spherical and globular bushy cells and the bushy multipolar neuron. They, too, represent a heterogeneous population. An onset neuron was identified as an octopus cell.

[1]  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.

[2]  W. S. Rhode,et al.  Physiological studies on neurons in the dorsal cochlear nucleus of cat. , 1986, Journal of neurophysiology.

[3]  M. Liberman Central projections of auditory‐nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus , 1991, The Journal of comparative neurology.

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

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

[6]  P. Manis,et al.  Outward currents in isolated ventral cochlear nucleus neurons , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[9]  Philip H Smith,et al.  Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: Evidence for delay lines to the medial superior olive , 1993, The Journal of comparative neurology.

[10]  N. Kiang,et al.  STIMULUS CODING AT CAUDAL LEVELS OF THE CAT'S AUDITORY NERVOUS SYSTEM: I. RESPONSE CHARACTERISTICS OF SINGLE UNITS , 1973 .

[11]  Joe C. Adams,et al.  Single unit studies on the dorsal and intermediate acoustic striae , 1976, The Journal of comparative neurology.

[12]  R. Britt,et al.  Synaptic events and discharge patterns of cochlear nucleus cells. I. Steady-frequency tone bursts. , 1976, Journal of neurophysiology.

[13]  J. Adams Heavy metal intensification of DAB-based HRP reaction product. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

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

[15]  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.

[16]  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.

[17]  Steven Greenberg,et al.  Physiology of the Cochlear Nuclei , 1992 .

[18]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

[19]  W. Shofner,et al.  Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. , 1988, Journal of neurophysiology.

[20]  W. S. Rhode,et al.  Encoding timing and intensity in the ventral cochlear nucleus of the cat. , 1986, Journal of neurophysiology.

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

[22]  R. R. Pfeiffer Anteroventral Cochlear Nucleus:Wave Forms of Extracellularly Recorded Spike Potentials , 1966, Science.

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

[24]  W. Brownell,et al.  Single unit analysis of the posteroventral cochlear nucleus of the decerebrate cat , 1982, Neuroscience.

[25]  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.

[26]  R. Perkins An electron microscopic study of synaptic organization in the medial superior olive of normal and experimental chinchillas , 1973, The Journal of comparative neurology.

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

[28]  D. K. Morest,et al.  Noise-induced degeneration in the brain and representation of inner and outer hair cells , 1983, Hearing Research.

[29]  PB Manis,et al.  Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  D. Oertel Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

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

[34]  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.

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

[36]  R. Batra,et al.  A physiological and structural study of neuron types in the cochlear nucleus. I. Intracellular responses to acoustic stimulation and current injection , 1994, The Journal of comparative neurology.

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

[38]  N. Yoshii,et al.  Several clinical aspects of thalamic pulvinotomy. , 1976, Applied neurophysiology.

[39]  E. Ostapoff,et al.  A degenerative disorder of the central auditory system of the gerbil , 1989, Hearing Research.

[40]  R. Perkins,et al.  A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarski optics , 1975, The Journal of comparative neurology.

[41]  D. Morest,et al.  Perfusion-fixation of the brain with chrome-osmium solutions for the rapid Golgi method. , 1966, The American journal of anatomy.

[42]  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.

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

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

[45]  R. Britt,et al.  Intracellular recordings from cat cochlear nucleus during tone stimulation. , 1970, Journal of neurophysiology.

[46]  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.

[47]  J. Willott,et al.  Morphology of the octopus cell area of the cochlear nucleus in young and aging C57BL/6J and CBA/J mice , 1990, The Journal of comparative neurology.

[48]  N. Kiang,et al.  STIMULUS CODING AT CAUDAL LEVELS OF THE CAT'S AUDITORY NERVOUS SYSTEM: II. PATTERNS OF SYNAPTIC ORGANIZATION , 1973 .

[49]  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.

[50]  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.

[51]  F. Krasne,et al.  Evidence for a computational distinction between proximal and distal neuronal inhibition. , 1992, Science.

[52]  E. Ostapoff,et al.  Synaptic organization of globular bushy cells in the ventral cochlear nucleus of the cat: A quantitative study , 1991, The Journal of comparative neurology.

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

[54]  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.

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

[56]  T. Yin,et al.  Interaural time sensitivity in medial superior olive of cat. , 1990, Journal of neurophysiology.

[57]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

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

[59]  R. Romand Intracellular recording of ‘chopper responses’ in the cochlear nucleus of the cat , 1979, Hearing Research.

[60]  Philip H Smith,et al.  Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat , 1991, The Journal of comparative neurology.

[61]  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.

[62]  R Meddis,et al.  A computer model of a cochlear-nucleus stellate cell: responses to amplitude-modulated and pure-tone stimuli. , 1992, The Journal of the Acoustical Society of America.

[63]  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.

[64]  D. Ryugo,et al.  Synaptic connections of the auditory nerve in cats: Relationship between endbulbs of held and spherical bushy cells , 1991, The Journal of comparative neurology.

[65]  M. Sachs,et al.  Regularity analysis in a compartmental model of chopper units in the anteroventral cochlear nucleus. , 1991, Journal of neurophysiology.

[66]  I. Winter,et al.  Responses of single units in the anteroventral cochlear nucleus of the guinea pig , 1990, Hearing Research.

[67]  J. E. Rose,et al.  Observations on phase-sensitive neurons of anteroventral cochlear nucleus of the cat: nonlinearity of cochlear output. , 1974, Journal of neurophysiology.

[68]  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.

[69]  D A Godfrey,et al.  Single unit activity in the dorsal cochlear nucleus of the cat , 1975, The Journal of comparative neurology.

[70]  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.

[71]  J. A. Hirsch,et al.  Intrinsic properties of neurones in the dorsal cochlear nucleus of mice, in vitro. , 1988, The Journal of physiology.

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