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An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig

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Summary

The distribution and colocalization of γ-aminobutyric acid (GABA)- and glycine-like immunoreactivity in the cochlear nuclear complex of the guinea pig have been studied to produce a light microscopic atlas. The method used was based on post-embedding immunocytochemistry in pairs of 0.5-μm-thick plastic sections treated with polyclonal antibodies against conjugated GABA and glycine respectively. Immunoreactive cells, presumably short axon neurones, predominated in the dorsal cochlear nucleus, with mostly single-GABA-labelled cells in the superficial layer, double-labelled in the middle, and single-glycine-labelled in the deep layers. A few large single-glycine-labelled cells, interpreted as commissural neurons, occurred in the ventral nucleus. Scattered double-labelled cells, probably Golgi cells, were seen in the granule cell domain. Immunolabelled puncta of all three staining categories occurred in large numbers throughout the complex, apposed to somata and in the neuropil, showing a differential distribution onto different types of neuron. Three immunolabelled tracts were noted: the tuberculoventral tract, the commissural acoustic stria, and the trapezoidal descending fibres. Most of the fibres in these tracts were single-labelled for glycine, although in the last mentioned tract single-GABA- and double-labelled fibres were also found. Some of the immunolabelled cell types described here are proposed as the origins of the similarly labelled puncta and fibres on the basis of known intrinsic connections.

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Abbreviations

1-4 :

DCN layers 1 to 4

as :

acoustic stria

AVCN :

anteroventral cochlear nucleus

C :

caudal

cap :

cap area

cas :

commissural acoustic stria

cnr :

cochlear nerve root

co :

commissural cell

CRVCN :

central region of the VCN

cw :

cartwheel cell

CZ :

confluence zone

d :

dendrite

D :

dorsal

das :

dorsal acoustic stria

DCN :

dorsal cochlear nucleus

df :

descending fibres

ep :

ependyma

flocc :

flocculus

g :

glial cell

GABA :

γ-aminobutyric acid

GLY :

glycine

gi :

giant cell

gl/gla :

globular cell/area

Go :

Golgi cell

gr :

granule cell

ias :

intermediate acoustic stria

icp :

inferior cerebellar peduncle

lam :

granule cell lamina

mp/mpa :

multipolar cell/area

oc/oca :

octopus cell/area

PVCN :

posteroventral cochlear nucleus

py :

pyramidal cell

R :

rostral

sgl :

superficial granule cell layer

spcg :

subpeduncular corner of granule cells

sph/spha :

spherical cell/area

st :

stellate cell

tb :

trapezoid body

tv :

tuberculoventral cell

TVT :

tuberculoventral tract

V :

ventral

VCN :

ventral cochlear nucleus

vn :

vestibular nerve

References

  • Adams JC, Mugnaini E (1987) Patterns of glutamate decarboxylase immunostaining in the feline cochlear nuclear complex studied with silver enhancement and electron microscopy. J Comp Neurol 262:375–401

    Google Scholar 

  • Benson CG, Potashner SJ (1990) Retrograde transport of [3H]-glycine from the cochlear nucleus to the superior olive in the guinea pig. J Comp Neurol 296:415–426

    Google Scholar 

  • Bergman M, Staatz-Benson C, Potashner SJ (1989) Amino acid uptake and release in the guinea pig cochlear nucleus after inferior colliculus ablation. Hear Res 42:283–292

    Google Scholar 

  • Berrebi AS, Mugnaini E (1991) Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat Embryol 183:427–454

    Google Scholar 

  • Burger PM, Hell J, Mehl E, Krasel C, Lottspeich F, Jahn R (1991) GABA and glycine in synaptic vesicles: storage and transport characteristics. Neuron 7:287–293

    Google Scholar 

  • Cant NB, Gaston KC (1982) Pathways connecting the right and left cochlear nuclei. J Comp Neurol 212:313–326

    Google Scholar 

  • Caspary DM (1990) Electrophysiological studies of glycinergic mechanisms in auditory brainstem structures. In: Ottersen OP, Storm-Mathisen J (eds) Glycine Neurotransmission. Wiley, Chichester, pp 453–483

    Google Scholar 

  • Caspary DM, Rybak LP, Faingold CL (1985) The effects of inhibitory and excitatory amino-acid neurotransmitters on the response properties of brainstem auditory neurons. In: Drescher DG (ed) Auditory Biochemistry. Thomas, Springfield Ill, pp 198–226

    Google Scholar 

  • Christensen H, Fykse EM, Fonnum F (1990) Uptake of glycine into synaptic vesicles isolated from the rat spinal cord. J Neurochem 54:1142–1147

    Google Scholar 

  • Dale N, Ottersen OP, Roberts A, Storm-Mathisen J (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324:255–257

    Google Scholar 

  • Evans EF, Nelson PG (1973) On the functional relationship between the dorsal and ventral divisions of the cochlear nucleus of the cat. Exp Brain Res 17:428–442

    Google Scholar 

  • Godfrey DA, Parli JA, Dunn JD, Ross CD (1988) Neurotransmitter microchemistry of the cochlear nucleus and superior olivary complex. In: Syka J, Masterton RB (eds) Auditory pathway. Structure and function. Plenum Press, New York, pp 107–1221

    Google Scholar 

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

    Google Scholar 

  • Helfert RH, Bonneau JM, Wenthold RJ, Altschuler RA (1989) GABA and glycine immunoreactivity in the guinea pig superior olivary complex. Brain Res 501:269–286

    Google Scholar 

  • Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in the cultured mouse brain neurones. Nature 325:529–531

    Google Scholar 

  • Juiz JM, Bonneau JM, Helfert RH, Wenthold RJ, Altschuler RA (1989) GABA and glycine immunoreactivities in the guinea pig cochlear nuclear complex: ultrastructural colabelling studies. In: Lim DJ (ed) Ass Res Otolaryng Abstr, Chicago, p 12

  • Klinke R, Boerger G, Gruber J (1969) Studies of the functional significance of efferent innervation in the auditory system: afferent neuronal activity as influenced by contralaterally applied sound. Pflügers Arch 306:165–175

    Google Scholar 

  • Lorente de Nó R (1933) Anatomy of the eighth nerve: III. General plan of structure of the primary cochlear nuclei. Laryngoscope 43:327–350

    Google Scholar 

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

    Google Scholar 

  • Moore JK (1986) Cochlear nuclei: relationship to the auditory nerve. In: Altschuler RA, Hoffman DW, Bobbin RP (eds) Neurobiology of hearing: the cochlea. Raven Press, New York, pp 283–301

    Google Scholar 

  • Moore JK, Moore RY (1987) Glutamic acid decarboxylase-like immunoreactivity in brainstem auditory nuclei of the rat. J Comp Neurol 260:157–174

    Google Scholar 

  • Moore JK, Osen KK (1990) Colocalization of GABA-like and glycine-like immunoreactivity in the cochlear nuclei of the baboon (Papio anubis). Soc Neurosci Abstr 16:716

    Google Scholar 

  • Mugnaini E (1985) GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: light and electron microscopic immunocytochemistry. J Comp Neurol 235:61–81

    Google Scholar 

  • Mugnaini E, Oertel WH (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunocytochemistry. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 4: GABA and neuropeptides in the CSN, Part I. Elsevier, Amsterdam, pp 436–608

    Google Scholar 

  • Mugnaini E, Osen KK, Dahl A-L, Friedrich VL Jr, 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

    Google Scholar 

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

    Google Scholar 

  • Oberdorfer MD, Parakkal MH, Altschuler RA, Wenthold RJ (1987) Co-localization of glycine and GABA in the cochlear nucleus. Soc Neurosci Abstr 13:544

    Google Scholar 

  • Oberdorfer MD, Parakkal MH, Altschuler RA, Wenthold RJ (1988) Ultrastructural localization of GABA-immunoreactive terminals in the anteroventral cochlear nucleus of the guinea pig. Hear Res 33:229–238

    Google Scholar 

  • Oertel D, Wu SH (1989) Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice. J Comp Neurol 283:228–247

    Google Scholar 

  • Oertel D, Wu SH, Garb MW, Dizack C (1990) Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J Comp Neurol 295:136–154

    Google Scholar 

  • Oliver DL (1984) Dorsal cochlear nucleus projections to the inferior colliculus in the cat: a light and electron microscopic study. J Comp Neurol 224:155–172

    Google Scholar 

  • Oliver DL (1985) Quantitative analyses of axonal endings in the central nucleus of the inferior colliculus and distribution of [3H]-labeling after injections in the dorsal cochlear nucleus. J Comp Neurol 237:343–359

    Google Scholar 

  • Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–484

    Google Scholar 

  • Osen KK (1985) “Ectopic” neurons in the cochlear nuclei. Neurosci Letters [Suppl 22]: S167

  • Osen KK, Mugnaini E, Dahl A-L, Christiansen AH (1984) Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei with emphasis on the cochlear granule cell system. Arch Ital Biol 122:169–212

    Google Scholar 

  • Osen KK, Ottersen OP, Storm-Mathisen J (1990) Colocalization of glycine-like and GABA-like immunoreactivities. A semiquantitative study of individual neurons in the dorsal cochlear nucleus of cat. In: Ottersen OP, Storm-Mathisen J (eds) Glycine neurotransmission. Wiley, Chichester, pp 417–451

    Google Scholar 

  • Osen KK, Lopez DE, Slyngstad TA, Ottersen OP, Storm-Mathisen J (1991) GABA-like and glycine-like immunoreactivities of the cochlear root nucleus in rat. J Neurocytol 20:17–25

    Google Scholar 

  • Ostapoff E-M, Morest DK (1991) Synaptic organization of globular bushy cells in the ventral cochlear nucleus of the cat: a quantitative study. J Comp Neurol 314:598–613

    Google Scholar 

  • Ostapoff E-M, Morest DK, Potashner SJ (1990) Uptake and retrograde transport of [3H]-GABA from the cochlear nucleus to the superior olive in the guinea pig. J Chem Neuroanat 3:285–295

    Google Scholar 

  • Ottersen OP (1987) Postembedding light- and electron microscopic immunocytochemistry of amino acids: description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp Brain Res 69:167–174

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J (1984a) Neurons containing or accumulating transmitter amino acids. In: Björklund A, Hökfelt T, Kuhar MJ (eds) Handbook of chemical neuroanatomy, vol 3. Classical transmitters and transmitter receptors in the CNS, Part II. Elsevier, Amsterdam, pp 141–246

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J (1984b) Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol 229:374–392

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J, Somogyi P (1988) Colocalization of glycine-like and GABA-like immunoreactivities in Golgi cell terminals in the rat cerebellum: a postembedding light and electron microscopic study. Brain Res 450:342–353

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J, Laake JH (1990) Cellular and subcellular localization of glycine studied by quantitative electron microscopic immunocytochemistry. In: Ottersen OP, Storm-Mathisen J (eds) Glycine neurotransmission. Wiley, Chichester, pp 303–328

    Google Scholar 

  • Pirsig W, Pfalz R, Sadanaga M (1968) Postsynaptic auditory crossed efferent inhibition in the ventral cochlear nucleus and its blocking by strychnine nitrate (guinea pig). Kumamoto Med J 21:75–82

    Google Scholar 

  • van den Pol AN, Gorcs T (1988) Glycine and glycine receptor immunoreactivity in brain and spinal cord. Neuroscience 8:472–492

    Google Scholar 

  • Potashner SJ, Lindberg N, Morest DK (1985) Uptake and release of γ-aminobutyric acid in the guinea pig cochlear nucleus after axotomy of cochlear and centrifugal fibers. J Neurochem 45:1558–1566

    Google Scholar 

  • Roberts RC, Ribak CE (1987) GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil. J Comp Neurol 258:267–280

    Google Scholar 

  • Saint Marie RL, Morest DK, Brandon CJ (1989) The form and distribution of GABAergic synapses on the principal cell types of the ventral cochlear nucleus of the cat. Hear Res 42:97–112

    Google Scholar 

  • Saint Marie RL, Benson CG, Ostapoff E-M, Morest DK (1991) Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus. Hear Res 51:11–28

    Google Scholar 

  • Schwartz IR, Yu S-M (1986) An anti-GABA antibody labels subpopulations of axonal terminals and neurons in the gerbil cochlear nucleus and superior olivary complex. Soc Neurosci Abstr 12:780

    Google Scholar 

  • Schwartz IR, Yu S-M, DiCarlantonio G, Wenthold RJ (1987) A comparison of GABA and glycine immunoreactivity in the gerbil dorsal cochlear nucleus. Soc Neurosci Abstr 13:544

    Google Scholar 

  • Semple MN, Aitkin LM (1980) Physiology of pathway from dorsal cochlear nucleus to inferior colliculus revealed by electrical and auditory stimulation. Exp Brain Res 41:19–28

    Google Scholar 

  • Shiraishi T, Senba E, Tohyama M, Wu J-Y, Kubo T, Matsunaga T (1985) Distribution and fine structure of neuronal elements containing glutamate decarboxylase in the rat cochlear nucleus. Brain Res 347:183–187

    Google Scholar 

  • Smith PH, Rhode WS (1985) Electron microscopic features of physiologically characterized, HRP-labeled fusiform cells in the cat dorsal cochlear nucleus. J Comp Neurol 237:127–143

    Google Scholar 

  • Smith PH, Rhode WS (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282:595–616

    Google Scholar 

  • Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu J-Y (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatinor cholecystokinin-immunoreactive material. J Neurosci 4:2590–2603

    Google Scholar 

  • Staatz-Benson C, Potashner SJ (1988) Uptake and release of glycine in the guinea pig cochlear nucleus after axotomy of afferent or centrifugal fibres. J Neurochem 51:370–379

    Google Scholar 

  • Storm-Mathisen J. Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug F-MS, Ottersen OP (1983) First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301:517–520

    Google Scholar 

  • Todd AJ, Sullivan AC (1990) Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296:496–505

    Google Scholar 

  • Triller A, Cluzeaud F, Seitanidou T (1990) Immunocytochemical localization of the glycine receptor. In: Ottersen OP, Storm-Mathisen J (eds) Glycine neurotransmission. Wiley, Chichester, pp 83–109

    Google Scholar 

  • Walberg F, Ottersen OP (1992) Neuroactive amino acids in the area postrema. An immunocytochemical investigation in rat with some observations in cat and monkey (Macaca fascicularis). Anat Embryol 185:529–545

    Google Scholar 

  • Wenthold RJ (1987) Evidence for a glycinergic pathway connecting the two cochlear nuclei: an immunohistochemical and retrograde transport study. Brain Res 415:183–187

    Google Scholar 

  • Wenthold RJ (1991) Neurotransmitters of auditory brainstem nuclei. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffman DW (eds) Neurobiology of hearing: the central auditory system. Raven Press, New York, pp 121–139

    Google Scholar 

  • Wenthold RJ, Hunter C (1990) Immunocytochemistry of glycine and glycine receptors in the central auditory system. In: Ottersen OP, Storm-Mathisen J (eds) Glycine neurotransmission. Wiley, Chichester, pp 391–416

    Google Scholar 

  • Wenthold RJ, Zempel JM, Parakkal MH, Reeks KA, Altschuler RA (1986) Immunocytochemical localisation of GABA in the cochlear nucleus of the guinea pig. Brain Res 380:7–18

    Google Scholar 

  • Wenthold RJ, Huie D, Altschuler RA, Reeks KA (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience 22:897–912

    Google Scholar 

  • Wickesberg RE, Oertel D (1988) Tonotopic projection from the dorsal to the anteroventral cochlear nucleus of mice. J Comp Neurol 268:389–399

    Google Scholar 

  • Wickesberg RE, Oertel D (1990) Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression. J Neurosci 10:1762–1768

    Google Scholar 

  • Wickesberg RE, Whitlon D, Oertel D (1991) Tuberculoventral neurons project to the multipolar cell area but not to the octopus cell area of the posteroventral cochlear nucleus. J Comp Neurol 313:457–468

    Google Scholar 

  • Wouterlood FG, Mugnaini E (1984) Cartwheel neurons of the dorsal cochlear nucleus: a Golgi-electron microscopic study in rat. J Comp Neurol 227:136–157

    Google Scholar 

  • Wouterlood FG, Mugnaini E, Osen KK, Dahl A-L (1984) Stellate neurons in rat dorsal cochlear nucleus studied with combined Golgi impregnation and electron microscopy: synaptic connections and mutual coupling by gap junctions. J Neurocytol 13:639–664

    Google Scholar 

  • Wu SH, Oertel D (1986) Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine. J Neurosci 6:2691–2706

    Google Scholar 

  • Zhang N, Walberg F, Laake JH, Meldrum BS, Ottersen OP (1990) Aspartate-like and glutamate-like immunoreactivities in the inferior olive and climbing fibre system: a light microscopic study in rat and baboon (Papio anubis). Neuroscience 38:61–80

    Google Scholar 

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Authors and Affiliations

  1. Department of Communication and Neuroscience, Keele University, ST5 5BG, Staffordshire, UK

    J. Kolston & C. M. Hackney

  2. Department of Anatomy, Institute of Basic Medical Sciences, University of Oslo, Blindern 0317, P.O. Box 1105, 3, N-Oslo, Norway

    K. K. Osen, O. P. Ottersen & J. Storm-Mathisen

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  1. J. Kolston
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  2. K. K. Osen
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  3. C. M. Hackney
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  4. O. P. Ottersen
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  5. J. Storm-Mathisen
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Kolston, J., Osen, K.K., Hackney, C.M. et al. An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat Embryol 186, 443–465 (1992). https://doi.org/10.1007/BF00185459

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