Acoustic and current-pulse responses of identified neurons in the dorsal cochlear nucleus of unanesthetized, decerebrate gerbils.

In an effort to establish relationships between cell physiology and morphology in the dorsal cochlear nucleus (DCN), intracellular single-unit recording and marking experiments were conducted on decerebrate gerbils using horseradish peroxidase (HRP)- or neurobiotin-filled micropipettes. Intracellular responses to acoustic (tone and broadband noise bursts) and electric current-pulse stimuli were recorded and associated with cell morphology. Units were classified according to the response map scheme (type I to type V). Results from 19 identified neurons, including 13 fusiform cells, 2 giant cells, and 4 cartwheel cells, reveal correlations between cell morphology of these neurons and their acoustic responses. Most fusiform cells (8/13) are associated with type III unit response properties. A subset of fusiform cells was type I/III units (2), type III-i units (2), and a type IV-T unit. The giant cells were associated with type IV-i unit response properties. Cartwheel cells all had weak acoustic responses that were difficult to classify. Some measures of membrane properties also were correlated with cell morphology but to a lesser degree. Giant cells and all but one fusiform cell fired only simple action potentials (APs), whereas all cartwheel cells discharged complex APs. Giant and fusiform cells all had monotonic rate versus current level curves, whereas cartwheel cells had nonmonotonic curves. This implies that inhibitory acoustic responses, resulting in nonmonotonic rate versus sound level curves, are due to local inhibitory interactions rather than strictly to membrane properties. A complex-spiking fusiform cell with type III unit properties suggests that cartwheel cells are not the only complex-spiking cells in DCN. The diverse response properties of the DCN's fusiform cells suggests that they are very sensitive to the specific complement of excitatory and inhibitory inputs they receive.

[1]  D. Lay The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents , 1972, Journal of morphology.

[2]  Ted,et al.  Address Reprint Requests To , 2008 .

[3]  K. A. Davis,et al.  Evidence of stimulus-dependent correlated activity in the dorsal cochlear nucleus of decerebrate gerbils. , 1997, Journal of neurophysiology.

[4]  H. Voigt,et al.  Evidence of inhibitory interactions between neurons in dorsal cochlear nucleus. , 1980, Journal of neurophysiology.

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

[6]  A. Ryan,et al.  Hearing sensitivity of the mongolian gerbil, Meriones unguiculatis. , 1976, The Journal of the Acoustical Society of America.

[7]  Eric D. Young,et al.  Response properties of type II and type III units in dorsal cochlear nucleus , 1982, Hearing Research.

[8]  H. Voigt,et al.  Intracellular response properties of units in the dorsal cochlear nucleus of unanesthetized decerebrate gerbil. , 1997, Journal of neurophysiology.

[9]  K. A. Davis,et al.  A statistically based method to generate response maps objectively , 1995, Journal of Neuroscience Methods.

[10]  I. Nelken,et al.  Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV units to narrowband and wideband stimuli. , 1994, Journal of neurophysiology.

[11]  Mnh,et al.  Histologie du Système Nerveux de Lʼhomme et des Vertébrés , 1998 .

[12]  D O Kim,et al.  Spontaneous and sound-evoked discharge characteristics of complex-spiking neurons in the dorsal cochlear nucleus of the unanesthetized decerebrate cat. , 1995, Journal of neurophysiology.

[13]  K. Osen Projection of the cochlear nuclei on the inferior colliculus in the cat , 1972, The Journal of comparative neurology.

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

[15]  H. Voigt,et al.  Response map properties of units in the dorsal cochlear nucleus of barbiturate-anesthetized gerbil (Meriones unguiculatus) , 1997, Hearing Research.

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

[17]  E D Young,et al.  Somatosensory effects on neurons in dorsal cochlear nucleus. , 1995, Journal of neurophysiology.

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

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

[20]  D. Ryugo,et al.  Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat , 1996, The Journal of comparative neurology.

[21]  R. Burkard,et al.  Comments on "Stimulus dependencies of the gerbil brain-stem auditory-evoked response (BAER). I: Effects of click level, rate and polarity" [J. Acoust. Soc. Am. 85, 2514-2525 (1989)]. , 1993, The Journal of the Acoustical Society of America.

[22]  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.

[23]  H. Voigt,et al.  Cross-correlation analysis of inhibitory interactions in dorsal cochlear nucleus. , 1990, Journal of neurophysiology.

[24]  S. Zhang,et al.  Tuberculoventral cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. , 1993, Journal of neurophysiology.

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

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

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

[28]  D. Oertel,et al.  Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  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.

[30]  E. S. Kane Autoradiographic evidence of primary projections to the caudal cochlear nucleus in cats. , 1977, The American journal of anatomy.

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

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

[33]  G. Spirou,et al.  Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus , 1994, The Journal of comparative neurology.

[34]  R. Burkard,et al.  Stimulus dependencies of the gerbil brain-stem auditory-evoked response (BAER). I: Effects of click level, rate, and polarity. , 1989, The Journal of the Acoustical Society of America.

[35]  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.

[36]  Eric D. Young,et al.  Identification of response properties of ascending axons from dorsal cochlear nucleus , 1980, Brain Research.

[37]  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.

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

[39]  E. Young,et al.  Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. , 1976, Journal of neurophysiology.

[40]  R. Frisina,et al.  Anatomy and physiology of the gerbil cochlear nucleus: An improved surgical approach for microelectrode studies , 1982, Hearing Research.

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

[42]  E D Young,et al.  Neural organization and responses to complex stimuli in the dorsal cochlear nucleus. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[43]  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.

[44]  D. Ryugo,et al.  Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: Mossy fiber endings and their targets , 1996, The Journal of comparative neurology.

[45]  S. Zhang,et al.  Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. , 1994, Journal of neurophysiology.

[46]  H. Voigt,et al.  Neuron labeling by extracellular delivery of horseradish peroxidase in vivo: a method for studying the local circuitry of projection and interneurons at physiologically characterized sites , 1995, Journal of Neuroscience Methods.

[47]  W. S. Rhode,et al.  Physiological study of neurons in the dorsal and posteroventral cochlear nucleus of the unanesthetized cat. , 1987, Journal of neurophysiology.

[48]  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.

[49]  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.

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

[51]  S. Zhang,et al.  Giant cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. , 1993, Journal of neurophysiology.

[52]  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.

[53]  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.

[54]  E. Ostapoff,et al.  A physiological and structural study of neuron types in the cochlear nucleus. II. Neuron types and their structural correlation with response properties , 1994, The Journal of comparative neurology.

[55]  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.

[56]  W. Plassmann,et al.  The cochlea in gerbilline rodents. , 1987, Brain, behavior and evolution.

[57]  K. A. Davis,et al.  Response properties of units in the dorsal cochlear nucleus of unanesthetized decerebrate gerbil. , 1996, Journal of neurophysiology.

[58]  S. Zhang,et al.  Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. , 1993, Journal of neurophysiology.

[59]  E D Young,et al.  Granule Cell Activation of Complex-Spiking Neurons in Dorsal Cochlear Nucleus , 1997, The Journal of Neuroscience.

[60]  E D Young,et al.  Excitatory/inhibitory response types in the cochlear nucleus: relationships to discharge patterns and responses to electrical stimulation of the auditory nerve. , 1985, Journal of neurophysiology.

[61]  M. Karnovsky,et al.  THF EARLY STAGES OF ABSORPTION OF INJECTED HORSERADISH PEROXIDASE IN THE PROXIMAL TUBULES OF MOUSE KIDNEY: ULTRASTRUCTURAL CYTOCHEMISTRY BY A NEW TECHNIQUE , 1966, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[62]  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.

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

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

[65]  Nace L. Golding,et al.  Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. , 1997, Journal of neurophysiology.

[66]  R. Gacek,et al.  The Primary Acoustic Nuclei , 1983 .