Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise‐induced hearing loss

Multisensory neurons in the dorsal cochlear nucleus (DCN) achieve their bimodal response properties [Shore (2005) Eur. J. Neurosci., 21, 3334–3348] by integrating auditory input via VIIIth nerve fibers with somatosensory input via the axons of cochlear nucleus granule cells [Shore et al. (2000) J. Comp. Neurol., 419, 271–285; Zhou & Shore (2004)J. Neurosci. Res., 78, 901–907]. A unique feature of multisensory neurons is their propensity for receiving cross‐modal compensation following sensory deprivation. Thus, we investigated the possibility that reduction of VIIIth nerve input to the cochlear nucleus results in trigeminal system compensation for the loss of auditory inputs. Responses of DCN neurons to trigeminal and bimodal (trigeminal plus acoustic) stimulation were compared in normal and noise‐damaged guinea pigs. The guinea pigs with noise‐induced hearing loss had significantly lower thresholds, shorter latencies and durations, and increased amplitudes of response to trigeminal stimulation than normal animals. Noise‐damaged animals also showed a greater proportion of inhibitory and a smaller proportion of excitatory responses compared with normal. The number of cells exhibiting bimodal integration, as well as the degree of integration, was enhanced after noise damage. In accordance with the greater proportion of inhibitory responses, bimodal integration was entirely suppressive in the noise‐damaged animals with no indication of the bimodal enhancement observed in a sub‐set of normal DCN neurons. These results suggest that projections from the trigeminal system to the cochlear nucleus are increased and/or redistributed after hearing loss. Furthermore, the finding that only neurons activated by trigeminal stimulation showed increased spontaneous rates after cochlear damage suggests that somatosensory neurons may play a role in the pathogenesis of tinnitus.

[1]  Jianxun Zhou,et al.  Projections from the trigeminal nuclear complex to the cochlear nuclei: A retrograde and anterograde tracing study in the guinea pig , 2004, Journal of neuroscience research.

[2]  M. Wallace,et al.  Sensory and Multisensory Responses in the Newborn Monkey Superior Colliculus , 2001, The Journal of Neuroscience.

[3]  J. Wepsic,et al.  Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. , 1966, Experimental neurology.

[4]  R. Illing,et al.  Acoustic trauma induces reemergence of the growth‐ and plasticity‐associated protein GAP‐43 in the rat auditory brainstem , 2002, The Journal of comparative neurology.

[5]  Tom C T Yin,et al.  Bimodal Interactions in the Superior Colliculus of the Behaving Cat , 2002, The Journal of Neuroscience.

[6]  Jinsheng Zhang,et al.  Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure , 2000, Hearing Research.

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

[8]  L. Hughes,et al.  Disruption of Lateral Efferent Pathways: Functional Changes in Auditory Evoked Responses , 2003, Journal of the Association for Research in Otolaryngology.

[9]  D. Caspary,et al.  Elevated Fusiform Cell Activity in the Dorsal Cochlear Nucleus of Chinchillas with Psychophysical Evidence of Tinnitus , 2002, The Journal of Neuroscience.

[10]  H. Francis,et al.  Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons , 2000, Hearing Research.

[11]  John J. Foxe,et al.  Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. , 2002, Journal of neurophysiology.

[12]  Jinsheng Zhang,et al.  Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure , 2004, Neuroscience Letters.

[13]  D. A. Godfrey,et al.  Connections between the cochlear nuclei in guinea pig , 1992, Hearing Research.

[14]  J. Lu,et al.  Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons , 2003, Neuroscience.

[15]  P. Kanold,et al.  A physiologically based model of discharge pattern regulation by transient K+ currents in cochlear nucleus pyramidal cells. , 2001, Journal of neurophysiology.

[16]  H. R. Clemo,et al.  Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a 'new' inhibitory form of multisensory convergence. , 2004, Cerebral cortex.

[17]  C. Bendotti,et al.  Distribution of GAP‐43 mRNA in the adult rat brain , 1993, The Journal of comparative neurology.

[18]  S. Shore,et al.  Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation , 2005, The European journal of neuroscience.

[19]  S. Potashner,et al.  Noise trauma alters D‐[3H]aspartate release and AMPA binding in chinchilla cochlear nucleus , 2004, Journal of neuroscience research.

[20]  S. Potashner,et al.  New Growth of Axons in the Cochlear Nucleus of Adult Chinchillas after Acoustic Trauma , 1997, Experimental Neurology.

[21]  M. Wallace,et al.  Representation and integration of multiple sensory inputs in primate superior colliculus. , 1996, Journal of neurophysiology.

[22]  S. Shore,et al.  Convergence of spinal trigeminal and cochlear nucleus projections in the inferior colliculus of the guinea pig , 2006, The Journal of comparative neurology.

[23]  Matthew Lewandowski,et al.  Cisplatin-induced hyperactivity in the dorsal cochlear nucleus and its relation to outer hair cell loss: relevance to tinnitus. , 2002, Journal of neurophysiology.

[24]  J. Kelly,et al.  Auditory cortex of the long-eared hedgehog (Hemiechinus auritus). I. Boundaries and frequency representation. , 1990, Brain, behavior and evolution.

[25]  A. Nuttall,et al.  Direct evidence of trigeminal innervation of the cochlear blood vessels , 1998, Neuroscience.

[26]  J. Janisse,et al.  Increases in spontaneous neural activity in the hamster dorsal cochlear nucleus following cisplatin treatment: a possible basis for cisplatin-induced tinnitus , 2002, Hearing Research.

[27]  S. Shore,et al.  External inferior colliculus integrates trigeminal and acoustic information: Unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig , 2006, Neuroscience Letters.

[28]  Dennis J. McFarland,et al.  Cutaneous-Evoked Tinnitus , 1999, Audiology and Neurotology.

[29]  John J. Foxe,et al.  Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. , 2000, Brain research. Cognitive brain research.

[30]  I. Winter,et al.  Temporal and mean rate discharge patterns of single units in the dorsal cochlear nucleus of the anesthetized guinea pig. , 1996, Journal of neurophysiology.

[31]  J A Kaltenbach,et al.  Neurophysiologic mechanisms of tinnitus. , 2000, Journal of the American Academy of Audiology.

[32]  Zvi Wollberg,et al.  Cross‐modal neuroplasticity in neonatally enucleated hamsters: structure, electrophysiology and behaviour , 2002, The European journal of neuroscience.

[33]  M. C. Brown,et al.  Postsynaptic Targets of Type II Auditory Nerve Fibers in the Cochlear Nucleus. , 2004, Journal of the Association for Research in Otolaryngology.

[34]  S. Potashner,et al.  Quantitative study of degeneration and new growth of axons and synaptic endings in the chinchilla cochlear nucleus after acoustic overstimulation , 2004, Journal of neuroscience research.

[35]  Michael M Merzenich,et al.  Local circuit properties underlying cortical reorganization. , 2002, Journal of neurophysiology.

[36]  Paul B. Manis,et al.  Transient Potassium Currents Regulate the Discharge Patterns of Dorsal Cochlear Nucleus Pyramidal Cells , 1999, The Journal of Neuroscience.

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

[38]  Jinsheng Zhang,et al.  Effects of cochlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucleus: implications for the origin of noise induced tinnitus , 2002, Hearing Research.

[39]  W. Precht.  The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

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

[41]  Z Vass,et al.  Trigeminal ganglion innervates the auditory brainstem , 2000, The Journal of comparative neurology.

[42]  A. Routtenberg,et al.  Activity-dependent regulation of axonal growth: posttranscriptional control of the GAP-43 gene by the NMDA receptor in developing hippocampus. , 1999, Journal of neurobiology.

[43]  D. Bodznick,et al.  An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish , 1994, Neuroscience Letters.

[44]  C. Schroeder,et al.  Somatosensory input to auditory association cortex in the macaque monkey. , 2001, Journal of neurophysiology.

[45]  C. Ori,et al.  Cerebral blood flow changes induced by electrical stimulation of the Gasserian ganglion after experimentally induced subarachnoid haemorrhage in pigs , 2005, Acta Neurochirurgica.

[46]  A. Møller,et al.  Some forms of tinnitus may involve the extralemniscal auditory pathway , 1992, The Laryngoscope.

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

[48]  R. Levine,et al.  CNS somatosensory-auditory interactions elicit or modulate tinnitus , 2003, Experimental Brain Research.

[49]  C. Haenggeli,et al.  Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat , 2005, The Journal of comparative neurology.

[50]  A. Møller,et al.  The non-classical auditory pathways are involved in hearing in children but not in adults , 2002, Neuroscience Letters.

[51]  D. A. Godfrey,et al.  Effects of acoustic trauma on dorsal cochlear nucleus neuron activity in slices , 2002, Hearing Research.

[52]  Auditory cortex of the long-eared hedgehog (Hemiechinus auritus): II. Tuning properties. , 1992, Brain, behavior and evolution.

[53]  Dennis J. McFarland,et al.  Cutaneous-Evoked Tinnitus , 1999, Audiology and Neurotology.

[54]  Jianxun Zhou,et al.  Somatosensory influence on the cochlear nucleus and beyond , 2006, Hearing Research.

[55]  S. Shore,et al.  Sources of input to the cochlear granule cell region in the guinea pig , 1998, Hearing Research.

[56]  F. Lepore,et al.  Auditory responses in the visual cortex of neonatally enucleated rats , 2007, Neuroscience.

[57]  S. Shore,et al.  Vessicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus , 2007, The Journal of comparative neurology.

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

[59]  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.

[60]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

[61]  L. Aitkin,et al.  The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus , 1981, The Journal of comparative neurology.