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PMID: 8224048 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology.

Experimental brain research ·Vol. 95 ·No. 2 ·1993-00-00 ·Pages 223-39

Sommer I, Lingenhöhl K, Friauf E

Abstract

The medial nucleus of the trapezoid body (MNTB) is one of several principal nuclei in the superior olivary complex (SOC) of mammals. It is classically thought to function as a relay station between the contralateral ventral cochlear nucleus and the lateral superior olive (LSO), playing a role among those brainstem nuclei that are involved in binaural hearing. In order to characterise the physiology and morphology at the cellular level of the major neuronal component of the MNTB, the principal cells, we have analysed these neurons in rats in vivo using intracellular recordings and horseradish peroxidase-labelling. Our data demonstrate that MNTB principal cells, when being stimulated acoustically via the contralateral ear, show a phasic-tonic response with an onset latency of 3.5 ms and a suppression of their spontaneous activity following stimulus offset. These neurons have an axonal morphology whose complexity has not yet been described. All cells (n = 10) projected exclusively ipsilaterally and had terminal axonal arbors in a variety of auditory brainstem nuclei. At least two and maximally seven auditory targets were innervated by an individual cell. Each cell projected into the LSO and the superior paraolivary nucleus (SPN). Additional projections that were intrinsic to the SOC were often observed in the lateral nucleus of the trapezoid body and in periolivary regions, with only one cell projecting into the medial superior olive. Most, if not all, MNTB principal cells also had projections that were extrinsic to the SOC, as their axons ascended into the lateral lemniscus. In two neurons the ascending axon formed terminal arbors in the ventral nucleus of the lateral lemniscus, and the dorsal nucleus of the lateral lemniscus could be identified as a target of one neuron. The location of the cell bodies of the MNTB principal cells correlated with the neurons' best frequencies, thereby demonstrating a tonotopic organisation of the MNTB, with high frequencies being represented medially and low frequencies laterally. The axonal projections into the LSO and the SPN were also tonotopically organised and the alignment of the tonotopically organised and the alignment of the tonotopic axes was similar to that in the MNTB. Our results confirm previous data from other species and suggest that MNTB principal cells have a great amount of physiological and morphological similarities across mammalian species. Furthermore, the complexity of the axonal projections indicates that these neurons play a role in auditory information processing which goes far beyond their previously described classical role.

MeSH Terms
Acoustic Stimulation Animals Auditory Pathways/cytology,physiology,ultrastructure Axons/physiology,ultrastructure Cochlear Nerve/cytology,physiology,ultrastructure Dendrites/ultrastructure Electrophysiology Female Histocytochemistry Horseradish Peroxidase Microelectrodes Pons/cytology,physiology,ultrastructure Rats Rats, Sprague-Dawley
Chemicals
Horseradish Peroxidase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sommer I
Department of Animal Physiology, University of Tübingen, Germany.
Lingenhöhl K
Friauf E
References (43)
43 references, click to expand
  1. Descending projections from auditory brainstem nuclei to the cochlea and cochlear nucleus of the guinea pig.
    J Comp Neurol. 1989 Feb 1;280(1):143-57 PMID: 2918093
  2. The projections of principal cells of the medial nucleus of the trapezoid body in the cat.
    J Comp Neurol. 1985 Aug 15;238(3):249-62 PMID: 4044914
  3. Evidence for an alteration of the tonotopic map in the gerbil cochlea during development.
    J Comp Neurol. 1989 Jan 15;279(3):436-44 PMID: 2918079
  4. Morphology of motoneurons in different subdivisions of the rat facial nucleus stained intracellularly with horseradish peroxidase.
    J Comp Neurol. 1986 Nov 8;253(2):231-41 PMID: 3793991
  5. Aging in the rat medial nucleus of the trapezoid body. I. Light microscopy.
    Neurobiol Aging. 1982 Fall;3(3):187-95 PMID: 6298647
  6. Organization of the superior olivary complex in the guinea pig. I. Cytoarchitecture, cytochrome oxidase histochemistry, and dendritic morphology.
    J Comp Neurol. 1991 Dec 22;314(4):645-70 PMID: 1726174
  7. Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body.
    J Neurosci. 1992 Jul;12(7):2819-37 PMID: 1351938
  8. Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat.
    Brain Res. 1972 May 26;40(2):247-70 PMID: 5027165
  9. Projections of the trapezoid body and the superior olivary complex of the Kangaroo rat (Dipodomys merriami).
    Brain Behav Evol. 1975;11(5-6):322-54 PMID: 1192176
  10. Tonotopic Order in the Adult and Developing Auditory System of the Rat as Shown by c-fos Immunocytochemistry.
    Eur J Neurosci. 1992;4(9):798-812 PMID: 12106303
  11. Heavy metal intensification of DAB-based HRP reaction product.
    J Histochem Cytochem. 1981 Jun;29(6):775 PMID: 7252134
  12. Application of coupled oxidation reaction to electron microscopic demonstration of horseradish peroxidase: cobalt-glucose oxidase method.
    Brain Res. 1979 Oct 19;175(2):341-6 PMID: 90544
  13. NMDA, non-NMDA and glycine receptors mediate binaural interaction in the lateral superior olive: physiological evidence from mouse brain slice.
    Neurosci Lett. 1992 Jan 6;134(2):257-60 PMID: 1350335
  14. Age-related loss of synaptic terminals in the rat medial nucleus of the trapezoid body.
    Neuroscience. 1988 Jan;24(1):189-94 PMID: 3368047
  15. Aging in the rat medial nucleus of the trapezoid body. II. Electron microscopy.
    J Comp Neurol. 1985 Feb 15;232(3):401-13 PMID: 3973099
  16. Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive.
    Hear Res. 1990 Nov;49(1-3):281-98 PMID: 2292501
  17. Ascending and intrinsic projections of the superior olivary complex in the cat.
    Exp Brain Res. 1978 May 12;32(1):117-34 PMID: 658183
  18. Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat.
    J Comp Neurol. 1991 Feb 15;304(3):387-407 PMID: 2022755
  19. The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus.
    Am J Anat. 1966 Mar;118(2):375-89 PMID: 5917192
  20. Development and specificity of inhibitory terminal arborizations in the central nervous system.
    J Neurobiol. 1991 Nov;22(8):837-54 PMID: 1663990
  21. The superior olivary complex in C57BL/6 mice.
    Am J Anat. 1979 Jul;155(3):349-73 PMID: 474450
  22. Classification of the principal cells of the medial nucleus of the trapezoid body.
    J Comp Neurol. 1991 Dec 22;314(4):707-20 PMID: 1816272
  23. Ascending auditory afferents to the nuclei of the lateral lemniscus.
    J Comp Neurol. 1981 Apr 20;197(4):673-703 PMID: 7229133
  24. A study of the cochlear nuclei and ascending auditory pathways of the medulla.
    J Comp Neurol. 1962 Dec;119:341-79 PMID: 13952992
  25. Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons.
    J Neurophysiol. 1990 May;63(5):1169-90 PMID: 2358868
  26. Different origins of cochlear efferents in some bat species, rats, and guinea pigs.
    J Comp Neurol. 1987 Oct 1;264(1):56-72 PMID: 3680624
  27. Auditory sensitivity of the albino rat.
    J Comp Physiol Psychol. 1977 Aug;91(4):930-6 PMID: 893752
  28. GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil.
    J Comp Neurol. 1987 Apr 8;258(2):267-80 PMID: 3584540
  29. Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance.
    J Comp Neurol. 1989 Jan 15;279(3):382-96 PMID: 2918077
  30. Afferents to the medial nucleus of the trapezoid body and their collateral projections.
    J Comp Neurol. 1991 Dec 22;314(4):684-706 PMID: 1816271
  31. Strychnine blocks binaural inhibition in lateral superior olivary neurons.
    J Neurosci. 1983 Jan;3(1):237-42 PMID: 6822858
  32. The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle.
    Brain Res. 1968 Jul;9(2):288-311 PMID: 5679830
  33. Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat.
    Hear Res. 1990 Nov;49(1-3):321-34 PMID: 2292504
  34. Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase.
    Exp Brain Res. 1988;73(2):263-84 PMID: 3215304
  35. A neuroanatomical study of the brainstem auditory system of the rabbit. I. Ascending connections.
    Acta Morphol Neerl Scand. 1973 Mar;11(1):31-48 PMID: 4121640
  36. Sensory neurons and motoneurons of the jaw-closing reflex pathway in rats: a combined morphological and physiological study using the intracellular horseradish peroxidase technique.
    Exp Brain Res. 1991;83(2):385-96 PMID: 1708725
  37. Intracellular labeling of afferents to the lateral superior olive in the bat, Eptesicus fuscus.
    Hear Res. 1988 Jul 15;34(2):141-7 PMID: 3170356
  38. The cytoarchitecture of the brain stem of the cat. I. Brain stem nuclei of cat.
    J Comp Neurol. 1961 Feb;116:27-69 PMID: 13774738
  39. The dual origins of the olivocochlear bundle in the albino rat.
    J Comp Neurol. 1983 Sep 10;219(2):203-14 PMID: 6619338
  40. Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat.
    J Comp Neurol. 1985 Feb 8;232(2):261-85 PMID: 3973093
  41. Single unit analysis of cat superior olive S segment with tonal stimuli.
    J Neurophysiol. 1966 Jul;29(4):684-97 PMID: 5966430
  42. Processing of binaural stimuli by cat superior olivary complex neurons.
    Exp Brain Res. 1983;52(3):385-99 PMID: 6653700
  43. Giant neurons in the caudal pontine reticular formation receive short latency acoustic input: an intracellular recording and HRP-study in the rat.
    J Comp Neurol. 1992 Nov 22;325(4):473-92 PMID: 1281843
Article Info
Journal
Experimental brain research
Abbr.
Exp Brain Res
ISSN
0014-4819
Published
1993-00-00
Pages
223-39
Language
English
Region
Germany
NLM ID
0043312
Subset
IM
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