Dual action of olivocochlear collaterals in the guinea pig cochlear nucleus

Axons of olivocochlear neurones in the superior olivary complex terminate on hair cells of the cochlea, reducing the sensitivity to sound. These axons also have collateral branches to neurones in the cochlear nucleus, the first processing centre in the brainstem. Anatomical data show that these collaterals terminate mainly in the granule cell area but their precise neuronal targets and the effects they might have are unknown. We have studied the effects of these collaterals in guinea pigs, by electrically stimulating the olivocochlear axons at the floor of the IVth ventricle while recording single neurone responses in the cochlear nucleus. We eliminated the peripheral effects of olivocochlear stimulation either by destruction of the target receptor cells using chronic administration of kanamycin, or by acute perfusion of the cochlea with strychnine, a specific blocker of the postsynaptic receptors. Electrical stimulation of the olivocochlear axons in normal animals caused a variety of effects on cochlear nucleus neurones. In some neurones, there was suppression of spontaneous firing and a reduction in sensitivity to sound, while in others there was an excitatory effect of olivocochlear axon stimulation. When the peripheral olivocochlear action was eliminated, we still found both inhibition and excitation in the cochlear nucleus. These results show that the effects of olivocochlear stimulation on cochlear nucleus responses are not a simple passive reflection of peripheral changes but are a result of complex interactions between peripheral suppression of afferent input and collateral-mediated excitation and possibly also inhibition.

[1]  B. Schofield Origins of projections from the inferior colliculus to the cochlear nucleus in guinea pigs , 2001, The Journal of comparative neurology.

[2]  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.

[3]  D. Ryugo,et al.  Pyramidal cells in primary auditory cortex project to cochlear nucleus in rat , 1996, Brain Research.

[4]  R. Illing,et al.  Olivocochlear neurons sending axon collaterals into the ventral cochlear nucleus of the rat , 2000 .

[5]  D. O. Kim,et al.  Marginal shell of the anteroventral cochlear nucleus: acoustically weakly-driven and not-driven units in the unanesthetized decerebrate cat. , 1996, Acta oto-laryngologica.

[6]  B. Schofield,et al.  Origins and targets of commissural connections between the cochlear nuclei in guinea pigs , 1996, The Journal of comparative neurology.

[7]  A. Starr,et al.  Olivocohlear bundle stimulation: effect on spontaneous and tone-evoked activities of single units in cat cochlear nucleus. , 1968, Journal of neurophysiology.

[8]  M B Sachs,et al.  Dynamic range of neural rate responses in the ventral cochlear nucleus of awake cats. , 1992, Journal of neurophysiology.

[9]  J. Puel Chemical synaptic transmission in the cochlea , 1995, Progress in Neurobiology.

[10]  D. Robertson,et al.  Effects on cochlear responses of activation of descending pathways from the inferior colliculus , 2000, Hearing Research.

[11]  D. Baguley,et al.  Mechanisms of tinnitus. , 2002, British medical bulletin.

[12]  R. Rajan Tonic activity of the crossed olivocochlear bundle in guinea pigs with idiopathic losses in auditory sensitivity , 1989, Hearing Research.

[13]  E D Young,et al.  Proprioceptive Information from the Pinna Provides Somatosensory Input to Cat Dorsal Cochlear Nucleus , 2001, The Journal of Neuroscience.

[14]  D. Ryugo,et al.  Glycine immunoreactivity of multipolar neurons in the ventral cochlear nucleus which project to the dorsal cochlear nucleus , 1999, The Journal of comparative neurology.

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

[16]  L. Alibardi,et al.  Ultrastructural and immunocytochemical characterization of commissural neurons in the ventral cochlear nucleus of the rat. , 1998, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[17]  Lionel Collet,et al.  On the role of the olivocochlear bundle in hearing: A case study , 1994, Hearing Research.

[18]  G. K. Yates,et al.  Cochlear action potential threshold and single unit thresholds. , 1979, The Journal of the Acoustical Society of America.

[19]  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.

[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]  M. Eybalin,et al.  Neurotransmitters and neuromodulators of the mammalian cochlea. , 1993, Physiological reviews.

[22]  A R Palmer,et al.  Level dependence of cochlear nucleus onset unit responses and facilitation by second tones or broadband noise. , 1995, Journal of neurophysiology.

[23]  Philip H Smith,et al.  Temporal and Binaural Properties in Dorsal Cochlear Nucleus and Its Output Tract , 1998, The Journal of Neuroscience.

[24]  John J. Guinan,et al.  Efferent innervation of the organ of corti: two separate systems , 1979, Brain Research.

[25]  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.

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

[27]  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.

[28]  D. Oertel,et al.  Cholinergic Modulation of Stellate Cells in the Mammalian Ventral Cochlear Nucleus , 2001, The Journal of Neuroscience.

[29]  N. Kiang,et al.  Effects of electric stimulation of the crossed olivocochlear bundle on single auditory-nerve fibers in the cat. , 1970, The Journal of the Acoustical Society of America.

[30]  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.

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

[32]  E. Keithley,et al.  Collaterals from lateral and medial olivocochhlear efferent neurons innervate different regions of the cochlear nucleus and adjacent brainstem , 1990, The Journal of comparative neurology.

[33]  S. Comis Centrifugal inhibitory processes affecting neurones in the cat cochlear nucleus , 1970, The Journal of physiology.

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

[35]  I. Winter,et al.  Descending projections from auditory brainstem nuclei to the cochlea and cochlear nucleus of the guinea pig , 1989, The Journal of comparative neurology.

[36]  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.

[37]  H. Ades,et al.  CYTOARCHITECTURE OF THE ORGAN OF CORTI. , 1964, Acta oto-laryngologica. Supplementum.

[38]  D. Caspary,et al.  Effects of acetylcholine on cochlear nucleus neurons , 1983, Experimental Neurology.

[39]  Z. Henderson,et al.  Cholinergic neurons in the ventral trapezoid nucleus project to the cochlear nuclei in the rat , 1994, Neuroscience.

[40]  C. Micheyl,et al.  Auditory efferents involved in speech‐in‐noise intelligibility , 1997, Neuroreport.

[41]  B. May,et al.  Effects of bilateral olivocochlear lesions on vowel formant discrimination in cats , 1998, Hearing Research.

[42]  W. Warr,et al.  Multiple projections from the ventral nucleus of the trapezoid body in the rat , 1996, Hearing Research.

[43]  R. Weinberg,et al.  A cuneocochlear pathway in the rat , 1987, Neuroscience.

[44]  M. Sachs,et al.  Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. , 1987, Journal of neurophysiology.

[45]  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.

[46]  M. Brown,et al.  Fiber pathways and branching patterns of biocytin‐labeled olivocochlear neurons in the mouse brainstem , 1993, The Journal of comparative neurology.

[47]  M. Charles Liberman,et al.  Effects of contralateral sound on auditory-nerve responses. II. Dependence on stimulus variables , 1989, Hearing Research.

[48]  R. Rajan Effect of electrical stimulation of the crossed olivocochlear bundle on temporary threshold shifts in auditory sensitivity. I. Dependence on electrical stimulation parameters. , 1988, Journal of neurophysiology.

[49]  D. Ryugo,et al.  Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats , 1997, The Journal of comparative neurology.

[50]  J. Desmedt Auditory-Evoked Potentials from Cochlea to Cortex as Influenced by Activation of the Efferent Olivo-Cochlear Bundle , 1962 .

[51]  T. E. Benson,et al.  Synaptic input to cochlear nucleus dendrites that receive medial olivocochlear synapses , 1996, The Journal of comparative neurology.

[52]  Duck O. Kim,et al.  Marginal shell of the anteroventral cochlear nucleus: intensity coding in single units of the unanesthetized, decerebrate cat , 1996, Neuroscience Letters.

[53]  I. Whitfield,et al.  Influence of centrifugal pathways on unit activity in the cochlear nucleus. , 1968, Journal of neurophysiology.