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Multimodal inputs to the granule cell domain of the cochlear nucleus

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Abstract

There is growing evidence that hearing involves the integration of many brain functions, including vision, balance, somatic sensation, learning and memory, and emotional state. Some of these integrative processes begin at the earliest stages of the central auditory system. In this review, we will discuss evidence that reveals multimodal projections into the granule cell domain of the cochlear nucleus.

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References

  • Adams JC (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183:519–538

    CAS  Google Scholar 

  • Aitkin LM (1973) Medial geniculate body of the cat: Responses to tonal stimuli of neurons in medial division. J Neurophysiol 36:275–283

    CAS  PubMed  Google Scholar 

  • Aitkin LM, Boyd J (1975) Responses of single units in cerebellar vermis of the cat to monaural and binaural stimuli. J Neurophysiol 38:418–429

    CAS  PubMed  Google Scholar 

  • Aitkin LM, Boyd J (1978) Acoustic input to the lateral pontine nuclei. Hear Res 1:67–77

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (1998) Ultrastructural and immunocytochemical characterization of neurons in the rat ventral cochlear nucleus projecting to the inferior colliculus. Ann Anat 180:415–426

    CAS  Google Scholar 

  • Alibardi L (2000) Cytology, synaptology and immunocytochemistry of commissural neurons and their putative axonal terminals in the dorsal cochlear nucleus of the rat. Ann Anat 182:207–220

    CAS  Google Scholar 

  • Alibardi L (2001) Fine structure and neurotransmitter cytochemistry of neurons in the rat ventral cochlear nucleus projecting to the ipsilateral dorsal cochlear nucleus. Ann Anat 183:459–469

    CAS  PubMed  Google Scholar 

  • Azizi SA, Woodward DJ (1990) Interactions of visual and auditory mossy fiber inputs in the paraflocculus of the rat: a gating action of multimodal inputs. Hear Res 533:255–262

    Article  CAS  Google Scholar 

  • Azizi SA, Burne RA, Woodward DJ (1985) The auditory corticopontocerebellar projection in the rat: inputs to the paraflocculus and midvermis. An anatomical and physiological study. Exp Brain Res 59:36–49

    CAS  PubMed  Google Scholar 

  • Bell CC, Bodznick D, Montgomery J, Bastian J (1997) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol 50:17–31

    PubMed  Google Scholar 

  • Bell CC, Han VZ, Sugawara Y, Grant K (1999) Synaptic plasticity in the mormyrid electrosensory lobe. J Exp Biol 202:1339–1347

    PubMed  Google Scholar 

  • Blackburn CC, Sachs MB (1989) Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis. J Neurophysiol 62:1303–1329

    CAS  PubMed  Google Scholar 

  • Brawer JR, Morest DK, Kane EC (1974) The neuronal architecture of the cochlear nucleus of the cat. J Comp Neurol 155:251–300

    CAS  PubMed  Google Scholar 

  • Brown MC, Liu TS (1995) Fos-like immunoreactivity in central auditory neurons of the mouse. J Comp Neurol 357:85–97

    CAS  PubMed  Google Scholar 

  • Brown MC, Berglund AM, Kiang NYS, Ryugo DK (1988) Central trajectories of type II spiral ganglion neurons. J Comp Neurol 278:581–590

    CAS  PubMed  Google Scholar 

  • Bukowska D (2002) Morphological evidence for secondary vestibular afferent connections to the dorsal cochlear nucleus in the rabbit. Cells Tissues Organs 170:61–68

    Article  CAS  PubMed  Google Scholar 

  • Burian M, Gstoettner W (1988) Projection of primary vestibular afferent fibers to the cochlear nucleus in the guinea pig. Neurosci Lett 84:13–17

    CAS  PubMed  Google Scholar 

  • Casseday HJ, Diamond IT, Harting JK (1976) Auditory pathways to the cortex in Tupaia glis. J Comp Neurol 166:303–340

    CAS  PubMed  Google Scholar 

  • Davis KA, Miller RL, Young ED (1996) Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus. J Neurophysiol 76:3012–3024

    CAS  PubMed  Google Scholar 

  • Devor A (2000) Is the cerebellum like cerebellar-like structures? Brain Res Rev 34:149–156

    CAS  PubMed  Google Scholar 

  • Doucet JR, Ryugo DK (1997) Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J Comp Neurol 385:245–264

    Article  CAS  PubMed  Google Scholar 

  • Ehret G, Fischer R (1991) Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression. Brain Res 567:350–354

    Article  CAS  PubMed  Google Scholar 

  • Erickson RP, Jane JA, Waite R, Diamond IT (1964) Single neuron investigation of sensory thalamus of the opossum. J Neurophysiol 27:1026–1047

    CAS  Google Scholar 

  • Evans EF, Nelson PG (1973) The responses of single neurones in the cochlear nucleus of the cat as a function of their location and anesthetic state. Exp Brain Res 17:402–427

    CAS  PubMed  Google Scholar 

  • Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol 175:35–52

    CAS  PubMed  Google Scholar 

  • Fekete DM, Rouiller EM, Liberman MC, Ryugo DK (1984) The central projections of intracellularly labeled auditory nerve fibers in cats. J Comp Neurol 229:432–450

    CAS  PubMed  Google Scholar 

  • Glendenning KK, Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) Ascending auditory afferents to the nuclei of the lateral lemniscus. J Comp Neurol 197:673–703

    CAS  PubMed  Google Scholar 

  • Glickstein M (1997) Mossy-fibre sensory input to the cerebellum. Prog Brain Res 114:251–259

    CAS  PubMed  Google Scholar 

  • Graybiel AM (1974) Studies on the anatomical organization of the posterior association cortex. In: Schmitt FO, Worden FG (eds) The Neurosciences Third Study Program. MIT Press, Cambridge, pp 205–214

  • Hackney CM, Osen KK, Kolston J (1990) Anatomy of the cochlear nuclear complex of guinea pig. Anat Embryol 182:123–149

    CAS  PubMed  Google Scholar 

  • Haenggeli C-A, Doucet JR, Ryugo DK (2002a) Trigeminal projections to the cochlear nucleus in rats. ARO Abstr 25:7

    Google Scholar 

  • Haenggeli C-A, Doucet JR, Ryugo DK (2002b) Projections of the spinal trigeminal nucleus to the cochlear nucleus. Proceedings of the Scientific Program, "Central auditory processing—integration with other systems", Monte-Verità, Switzerland, P36

  • Huang C-M, Liu L, Pettavel P, Huang RH (1990) Target areas of presumed auditory projections from lateral and dorsolateral pontine nuclei to posterior cerebellar vermis in rat. Brain Res 536:327–330

    Article  CAS  PubMed  Google Scholar 

  • Hurd LB, Hutson KA, Morest DK (1999) Cochlear nerve projections to the small cell shell of the cochlear nucleus: the neuroanatomy of extremely thin sensory axons. Synapse 33:83–117

    Article  CAS  PubMed  Google Scholar 

  • Itoh K, Kamiya H, Mitani A, Yasui Y, Takada M, Mizuno N (1987) Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat. Brain Res 400:145–150

    Article  CAS  PubMed  Google Scholar 

  • Kamada T, Wu M, Jen H-S (1992) Auditory response properties and spatial response areas of single neurons in the pontine nuclei of the big brown bat. Brain Res 575:187–198

    CAS  PubMed  Google Scholar 

  • Kandler K, Herbert H (1991) Auditory projections from the cochlear nucleus to pontine and mesencephalic reticular nuclei in the rat. Brain Res 562:230–242

    Article  CAS  PubMed  Google Scholar 

  • Kanold PO, Young ED (2001) Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 21:7848–7858

    CAS  PubMed  Google Scholar 

  • Kawamura K (1975) The pontine projection from the inferior colliculus in the cat. An experimental anatomical study. Brain Res 95:309–322

    Article  CAS  PubMed  Google Scholar 

  • Kevetter GA, Perachio AA (1989) Projections from the sacculus to the cochlear nuclei in the Mongolian gerbil. Brain Behav Evol 34:193–200

    CAS  PubMed  Google Scholar 

  • Knowlton BJ, Thompson JK, Thompson RF (1993) Projections from the auditory cortex to the pontine nuclei in the rabbit. Behav Brain Res 56:23–30

    Article  CAS  PubMed  Google Scholar 

  • Lorente de Nó R (1938) The cerebral cortex: architecture, intracortical connections, motor projections. In: Fulton JF (ed) Physiology of the nervous system. Oxford University Press, New York, pp 291–340

  • Lorente de Nó R (1981) The primary acoustic nuclei. Raven Press, New York

  • Love JA, Scott JW (1969) Some response characteristics of cells of the magnocellular division of the medial geniculate body of the cat. Can J Physiol Pharm 47:881–888

    CAS  Google Scholar 

  • Lund RD, Webster KE (1967a) Thalamic afferents from the dorsal column nuclei. An experimental anatomical study in the rat. J Comp Neurol 130:301–312

    CAS  PubMed  Google Scholar 

  • Lund RD, Webster KE (1967b) Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat. J Comp Neurol 130:313–328

    CAS  PubMed  Google Scholar 

  • Maslany S, Crockett DP, Egger MD (1991) Somatotopic organization of the dorsal column nuclei in the rat: transganglionic labelling with B-HRP and WGA-HRP. Brain Res 564:56–65

    Article  CAS  PubMed  Google Scholar 

  • McCrea RA, Strassman A, May E, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 264:547–570

    CAS  PubMed  Google Scholar 

  • McDonald DM, Rasmussen GL (1971) Ultrastructural characteristics of synaptic endings in the cochlear nucleus having acetylcholinesterase activity. Brain Res 28:1–18

    Article  CAS  PubMed  Google Scholar 

  • Middlebrooks JC, Makous JC, Green DM (1989) Directional sensitivity of sound-pressure levels in the human ear canal. J Acoust Soc Am 59:89–108

    Google Scholar 

  • Mihailoff GA, McArdle CB, Adams CE (1981) The cytoarchitecture, cytology, and synaptic organization of the basilar pontine nuclei in the rat. I. Nissl and Golgi studies. J Comp Neurol 195:181–201

    Google Scholar 

  • Millar J, Basbaum AI (1975) Topography of the projection of the body surface of the cat to cuneate and gracile nuclei. Exp Neurol 49:281–290

    CAS  PubMed  Google Scholar 

  • Mugnaini E, Morgan JI (1987) The neuropeptide cerebellin is a marker for two similar neuronal circuits in rat brain. Proc Natl Acad Sci 84:8692–8696

    CAS  PubMed  Google Scholar 

  • Mugnaini E, Osen KK, Dahl AL, Friedrich Jr. VL, Korte G (1980a) Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat, and mouse. J Neurocytol 9:537–570

    CAS  PubMed  Google Scholar 

  • Mugnaini E, Warr WB, Osen KK (1980b) Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse. J Comp Neurol 191:581–606

    CAS  PubMed  Google Scholar 

  • Musicant AD, Chan JCK, Hind JE (1990) Direction-dependent spectral properties of cat external ear: New data and cross-species comparisons. J Acoust Soc Am 87:757–781

    CAS  PubMed  Google Scholar 

  • Ohlrogge M, Doucet JR, Ryugo DK (2001) Projections of the pontine nuclei to the cochlear nucleus in rats. J Comp Neurol 436:290–303

    Article  CAS  PubMed  Google Scholar 

  • Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–482

    CAS  PubMed  Google Scholar 

  • Palay SL, Chan-Palay V (1974) Cerebellar cortex, cytology and organization. Springer-Verlag, New York

  • Pfaller K, Arvidsson J (1988) Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J Comp Neurol 268:91–108

    CAS  PubMed  Google Scholar 

  • Pfeiffer RR (1966) Classification of response patterns of spike discharges for units in the cochlear nucleus: tone burst stimulation. Exp Brain Res 1:220–235

    CAS  PubMed  Google Scholar 

  • Populin LC, Yin TCT (1995) Topographical organization of the motoneuron pools that innervate the muscles of the pinna of the cat. J Comp Neurol 363:600–614

    CAS  PubMed  Google Scholar 

  • Potter RF, Rüegg DG, Wiesendanger M (1978) Responses of neurons of the pontine nuclei to stimulation of the sensorimotor, visual and auditory cortex of rats. Brain Res Bull 3:15–19

    CAS  PubMed  Google Scholar 

  • Prihoda M, Hiller M-S, Mayr R (1991) Central projections of cervical primary afferent fibers in the guinea pig: an HRP and WGA/HRP tracer study. J Comp Neurol 308:418–431

    CAS  PubMed  Google Scholar 

  • Qian Y, Jen H-S (1994) Fos-like immunoreactivity elicited by sound stimulation in the auditory neurons of the big brown bat Eptesicus fuscus. Brain Res 664:241–246

    Article  CAS  PubMed  Google Scholar 

  • Ramón y Cajal R (1909) Histologie du Système Nerveux de l'Homme et des Vertébrés. Instituto Ramón y Cajal, Madrid

  • Rice JJ, May BJ, Spirou GA, Young ED (1992) Pinna-based spectral cues for sound localization in cat. Hear Res 58:132–152

    Article  CAS  PubMed  Google Scholar 

  • RoBards MJ (1979) Somatic neurons in the brainstem and neocortex projecting to the external nucleus of the inferior colliculus: anatomical study in the opossum. J Comp Neurol 184:547–566

    CAS  PubMed  Google Scholar 

  • Roth GL, Aitken LM, Anderson RA, Merzenich MM (1978) Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 182:661–680

    CAS  PubMed  Google Scholar 

  • Rouiller EM, Wan XST, Moret V, Liang F (1992) Mapping of c-fos expression elicited by pure tone stimulation in the auditory pathways of the rat, with emphasis on the cochlear nucleus. Neurosci Lett 144:19–24

    Article  CAS  PubMed  Google Scholar 

  • Ryugo DK, Weinberger NM (1978) Differential plasticity of morphologically distinct neuron populations in the medical geniculate body of the cat during classical conditioning. Behav Biol 22:275–301

    CAS  PubMed  Google Scholar 

  • Ryugo DK, Willard FH (1985) The dorsal cochlear nucleus of the mouse: A light microscopic analysis of neurons that project to the inferior colliculus. J Comp Neurol 242:381–396

    CAS  PubMed  Google Scholar 

  • Schofield BR (1995) Projections from the cochlear nucleus to the superior paraolivary nucleus in guinea pigs. J Comp Neurol 360:135–149

    CAS  PubMed  Google Scholar 

  • Schofield BR, Cant NB (1996a) Origins and targets of commissural connections between the cochlear nuclei in guinea pigs. J Comp Neurol 375:128–146

    Article  CAS  PubMed  Google Scholar 

  • Schofield BR, Cant NB (1996b) Projections from the ventral cochlear nucleus to the inferior colliculus and the contralateral cochlear nucleus in guinea pigs. Hear Res 102:1–14

    Article  CAS  PubMed  Google Scholar 

  • Schroeder DM, Jane JA (1971) Projections of the dorsal column nuclei and spinal cord to brain stem and thalamus in the tree shrew (Tupaia glis). J Comp Neurol 142:309–350

    CAS  PubMed  Google Scholar 

  • Shaw EAG (1982) External ear response and sound localization. In: Gatehouse RW (ed) Localization of sound: theory and applications. Amphora, Groton, pp 30–42

  • Shore SE, Vass Z, Wys NL, Altschuler RA (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419:271–285

    CAS  PubMed  Google Scholar 

  • Swanson LW (1992) Brain maps: structure of the rat brain. Elsevier, Amsterdam

    Google Scholar 

  • Walsh TM, Ebner F (1973) Distribution of the cerebellar and somatic lemniscal projections in the ventral nucleus complex of the Virginia opossum. J Comp Neurol 147:427–446

    CAS  PubMed  Google Scholar 

  • Warr WB (1982) Parallel ascending pathways from the cochlear nucleus: Neuroanatomical evidence of functional specialization. In: Neff WD (ed) Contributions to sensory physiology, vol 7. Academic Press, New York, pp 1–38

  • Weedman DL, Pongstaporn T, Ryugo DK (1996) Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: Mossy fiber endings and their targets. J Comp Neurol 369:345–360

    Article  CAS  PubMed  Google Scholar 

  • Weinberg RJ, Rustioni A (1987) A cuneocochlear pathway in the rat. Neuroscience 20:209–219

    Article  CAS  PubMed  Google Scholar 

  • Wepsic JG (1966) Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. Exp Neurol 15:299–318

    CAS  PubMed  Google Scholar 

  • Wright DD, Ryugo DK (1996) Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. J Comp Neurol 365:159–172

    Article  CAS  PubMed  Google Scholar 

  • Young ED, Brownell WE (1976) Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J Neurophysiol 39:282–300

    CAS  PubMed  Google Scholar 

  • Young ED, Shofner WP, White JA, Robert J-M, Voigt HF (1988) Response properties of cochlear nucleus neurons in relationship to physiological mechanisms. In: Edelman GM, Gall WE, Cowan WM (eds) Auditory function: neurobiological bases of hearing. Wiley, New York, pp 277–312

  • Young ED, Nelken I, Conley RA (1995) Somatosensory effects on neurons in dorsal cochlear nucleus. J Neurophysiol 73:743–765

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank the past and present investigators who have contributed knowledge to this topic, especially those from our own laboratory which include Debora Wright Tingley, Diana Weedman Molavi, Liana Rose, Matthias Ohlrogge, Kate Chefer, Tan Pongstaporn, Alison Wright, Jenna Los, and Xiping Zhan. Supported by grants from NIH/NIDCD DC00232, DC04395, DC04505, and the Schweizerishe Stiftung für Medizinisch-Biologische Stipendien.

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  1. Center for Hearing Sciences, Department of Otolaryngology-HNS, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Baltimore, MD 21205, USA

    David K. Ryugo, Charles-André Haenggeli & John R. Doucet

  2. Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA

    David K. Ryugo

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  1. David K. Ryugo
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  2. Charles-André Haenggeli
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  3. John R. Doucet
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Correspondence to David K. Ryugo.

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Ryugo, D.K., Haenggeli, CA. & Doucet, J.R. Multimodal inputs to the granule cell domain of the cochlear nucleus. Exp Brain Res 153, 477–485 (2003). https://doi.org/10.1007/s00221-003-1605-3

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