Experimental Brain Research

, Volume 153, Issue 4, pp 477–485 | Cite as

Multimodal inputs to the granule cell domain of the cochlear nucleus

  • David K. Ryugo
  • Charles-André Haenggeli
  • John R. Doucet
Review

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.

Keywords

Audition Mossy fibers Sensory integration Synapses 

Notes

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.

References

  1. Adams JC (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183:519–538Google Scholar
  2. Aitkin LM (1973) Medial geniculate body of the cat: Responses to tonal stimuli of neurons in medial division. J Neurophysiol 36:275–283PubMedGoogle Scholar
  3. Aitkin LM, Boyd J (1975) Responses of single units in cerebellar vermis of the cat to monaural and binaural stimuli. J Neurophysiol 38:418–429PubMedGoogle Scholar
  4. Aitkin LM, Boyd J (1978) Acoustic input to the lateral pontine nuclei. Hear Res 1:67–77CrossRefPubMedGoogle Scholar
  5. Alibardi L (1998) Ultrastructural and immunocytochemical characterization of neurons in the rat ventral cochlear nucleus projecting to the inferior colliculus. Ann Anat 180:415–426Google Scholar
  6. 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 182:207–220Google Scholar
  7. 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 183:459–469PubMedGoogle Scholar
  8. 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 533:255–262CrossRefGoogle Scholar
  9. 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 59:36–49PubMedGoogle Scholar
  10. Bell CC, Bodznick D, Montgomery J, Bastian J (1997) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol 50:17–31PubMedGoogle Scholar
  11. Bell CC, Han VZ, Sugawara Y, Grant K (1999) Synaptic plasticity in the mormyrid electrosensory lobe. J Exp Biol 202:1339–1347PubMedGoogle Scholar
  12. Blackburn CC, Sachs MB (1989) Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis. J Neurophysiol 62:1303–1329PubMedGoogle Scholar
  13. Brawer JR, Morest DK, Kane EC (1974) The neuronal architecture of the cochlear nucleus of the cat. J Comp Neurol 155:251–300PubMedGoogle Scholar
  14. Brown MC, Liu TS (1995) Fos-like immunoreactivity in central auditory neurons of the mouse. J Comp Neurol 357:85–97PubMedGoogle Scholar
  15. Brown MC, Berglund AM, Kiang NYS, Ryugo DK (1988) Central trajectories of type II spiral ganglion neurons. J Comp Neurol 278:581–590PubMedGoogle Scholar
  16. Bukowska D (2002) Morphological evidence for secondary vestibular afferent connections to the dorsal cochlear nucleus in the rabbit. Cells Tissues Organs 170:61–68CrossRefPubMedGoogle Scholar
  17. Burian M, Gstoettner W (1988) Projection of primary vestibular afferent fibers to the cochlear nucleus in the guinea pig. Neurosci Lett 84:13–17PubMedGoogle Scholar
  18. Casseday HJ, Diamond IT, Harting JK (1976) Auditory pathways to the cortex in Tupaia glis. J Comp Neurol 166:303–340PubMedGoogle Scholar
  19. Davis KA, Miller RL, Young ED (1996) Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus. J Neurophysiol 76:3012–3024PubMedGoogle Scholar
  20. Devor A (2000) Is the cerebellum like cerebellar-like structures? Brain Res Rev 34:149–156PubMedGoogle Scholar
  21. Doucet JR, Ryugo DK (1997) Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J Comp Neurol 385:245–264CrossRefPubMedGoogle Scholar
  22. Ehret G, Fischer R (1991) Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression. Brain Res 567:350–354CrossRefPubMedGoogle Scholar
  23. Erickson RP, Jane JA, Waite R, Diamond IT (1964) Single neuron investigation of sensory thalamus of the opossum. J Neurophysiol 27:1026–1047Google Scholar
  24. 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 17:402–427PubMedGoogle Scholar
  25. Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol 175:35–52PubMedGoogle Scholar
  26. Fekete DM, Rouiller EM, Liberman MC, Ryugo DK (1984) The central projections of intracellularly labeled auditory nerve fibers in cats. J Comp Neurol 229:432–450PubMedGoogle Scholar
  27. Glendenning KK, Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) Ascending auditory afferents to the nuclei of the lateral lemniscus. J Comp Neurol 197:673–703PubMedGoogle Scholar
  28. Glickstein M (1997) Mossy-fibre sensory input to the cerebellum. Prog Brain Res 114:251–259PubMedGoogle Scholar
  29. 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 205–214Google Scholar
  30. Hackney CM, Osen KK, Kolston J (1990) Anatomy of the cochlear nuclear complex of guinea pig. Anat Embryol 182:123–149PubMedGoogle Scholar
  31. Haenggeli C-A, Doucet JR, Ryugo DK (2002a) Trigeminal projections to the cochlear nucleus in rats. ARO Abstr 25:7Google Scholar
  32. 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, P36Google Scholar
  33. 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 536:327–330CrossRefPubMedGoogle Scholar
  34. 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 33:83–117CrossRefPubMedGoogle Scholar
  35. 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 400:145–150CrossRefPubMedGoogle Scholar
  36. 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 575:187–198PubMedGoogle Scholar
  37. Kandler K, Herbert H (1991) Auditory projections from the cochlear nucleus to pontine and mesencephalic reticular nuclei in the rat. Brain Res 562:230–242CrossRefPubMedGoogle Scholar
  38. Kanold PO, Young ED (2001) Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 21:7848–7858PubMedGoogle Scholar
  39. Kawamura K (1975) The pontine projection from the inferior colliculus in the cat. An experimental anatomical study. Brain Res 95:309–322CrossRefPubMedGoogle Scholar
  40. Kevetter GA, Perachio AA (1989) Projections from the sacculus to the cochlear nuclei in the Mongolian gerbil. Brain Behav Evol 34:193–200PubMedGoogle Scholar
  41. Knowlton BJ, Thompson JK, Thompson RF (1993) Projections from the auditory cortex to the pontine nuclei in the rabbit. Behav Brain Res 56:23–30CrossRefPubMedGoogle Scholar
  42. 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 291–340Google Scholar
  43. Lorente de Nó R (1981) The primary acoustic nuclei. Raven Press, New YorkGoogle Scholar
  44. 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 47:881–888Google Scholar
  45. Lund RD, Webster KE (1967a) Thalamic afferents from the dorsal column nuclei. An experimental anatomical study in the rat. J Comp Neurol 130:301–312PubMedGoogle Scholar
  46. Lund RD, Webster KE (1967b) Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat. J Comp Neurol 130:313–328PubMedGoogle Scholar
  47. 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 564:56–65CrossRefPubMedGoogle Scholar
  48. 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 264:547–570PubMedGoogle Scholar
  49. McDonald DM, Rasmussen GL (1971) Ultrastructural characteristics of synaptic endings in the cochlear nucleus having acetylcholinesterase activity. Brain Res 28:1–18CrossRefPubMedGoogle Scholar
  50. Middlebrooks JC, Makous JC, Green DM (1989) Directional sensitivity of sound-pressure levels in the human ear canal. J Acoust Soc Am 59:89–108Google Scholar
  51. 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 195:181–201Google Scholar
  52. Millar J, Basbaum AI (1975) Topography of the projection of the body surface of the cat to cuneate and gracile nuclei. Exp Neurol 49:281–290PubMedGoogle Scholar
  53. Mugnaini E, Morgan JI (1987) The neuropeptide cerebellin is a marker for two similar neuronal circuits in rat brain. Proc Natl Acad Sci 84:8692–8696PubMedGoogle Scholar
  54. 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 9:537–570PubMedGoogle Scholar
  55. 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 191:581–606PubMedGoogle Scholar
  56. 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 87:757–781PubMedGoogle Scholar
  57. Ohlrogge M, Doucet JR, Ryugo DK (2001) Projections of the pontine nuclei to the cochlear nucleus in rats. J Comp Neurol 436:290–303CrossRefPubMedGoogle Scholar
  58. Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–482PubMedGoogle Scholar
  59. Palay SL, Chan-Palay V (1974) Cerebellar cortex, cytology and organization. Springer-Verlag, New YorkGoogle Scholar
  60. 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 268:91–108PubMedGoogle Scholar
  61. Pfeiffer RR (1966) Classification of response patterns of spike discharges for units in the cochlear nucleus: tone burst stimulation. Exp Brain Res 1:220–235PubMedGoogle Scholar
  62. Populin LC, Yin TCT (1995) Topographical organization of the motoneuron pools that innervate the muscles of the pinna of the cat. J Comp Neurol 363:600–614PubMedGoogle Scholar
  63. 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 3:15–19PubMedGoogle Scholar
  64. 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 308:418–431PubMedGoogle Scholar
  65. 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 664:241–246CrossRefPubMedGoogle Scholar
  66. Ramón y Cajal R (1909) Histologie du Système Nerveux de l'Homme et des Vertébrés. Instituto Ramón y Cajal, MadridGoogle Scholar
  67. Rice JJ, May BJ, Spirou GA, Young ED (1992) Pinna-based spectral cues for sound localization in cat. Hear Res 58:132–152CrossRefPubMedGoogle Scholar
  68. 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 184:547–566PubMedGoogle Scholar
  69. 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 182:661–680PubMedGoogle Scholar
  70. 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 144:19–24CrossRefPubMedGoogle Scholar
  71. 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 22:275–301PubMedGoogle Scholar
  72. 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 242:381–396PubMedGoogle Scholar
  73. Schofield BR (1995) Projections from the cochlear nucleus to the superior paraolivary nucleus in guinea pigs. J Comp Neurol 360:135–149PubMedGoogle Scholar
  74. Schofield BR, Cant NB (1996a) Origins and targets of commissural connections between the cochlear nuclei in guinea pigs. J Comp Neurol 375:128–146CrossRefPubMedGoogle Scholar
  75. 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 102:1–14CrossRefPubMedGoogle Scholar
  76. 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 142:309–350PubMedGoogle Scholar
  77. Shaw EAG (1982) External ear response and sound localization. In: Gatehouse RW (ed) Localization of sound: theory and applications. Amphora, Groton, pp 30–42Google Scholar
  78. Shore SE, Vass Z, Wys NL, Altschuler RA (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419:271–285PubMedGoogle Scholar
  79. Swanson LW (1992) Brain maps: structure of the rat brain. Elsevier, AmsterdamGoogle Scholar
  80. 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 147:427–446PubMedGoogle Scholar
  81. 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 1–38Google Scholar
  82. 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 369:345–360CrossRefPubMedGoogle Scholar
  83. Weinberg RJ, Rustioni A (1987) A cuneocochlear pathway in the rat. Neuroscience 20:209–219CrossRefPubMedGoogle Scholar
  84. Wepsic JG (1966) Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. Exp Neurol 15:299–318PubMedGoogle Scholar
  85. Wright DD, Ryugo DK (1996) Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. J Comp Neurol 365:159–172CrossRefPubMedGoogle Scholar
  86. Young ED, Brownell WE (1976) Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J Neurophysiol 39:282–300PubMedGoogle Scholar
  87. 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 277–312Google Scholar
  88. Young ED, Nelken I, Conley RA (1995) Somatosensory effects on neurons in dorsal cochlear nucleus. J Neurophysiol 73:743–765PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • David K. Ryugo
    • 1
    • 2
  • Charles-André Haenggeli
    • 1
  • John R. Doucet
    • 1
  1. 1.Center for Hearing Sciences, Department of Otolaryngology-HNSJohns Hopkins University School of MedicineBaltimoreUSA
  2. 2.Department of NeuroscienceJohns Hopkins University School of MedicineBaltimoreUSA

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