Elsevier

Neuroscience

Volume 163, Issue 1, 29 September 2009, Pages 372-387
Neuroscience

Sensory System
Research Paper
Connections of the superior paraolivary nucleus of the rat: projections to the inferior colliculus

https://doi.org/10.1016/j.neuroscience.2009.06.030Get rights and content

Abstract

GABAergic neurotransmission contributes to shaping the response properties of inferior colliculus (IC) neurons. In rodents, the superior paraolivary nucleus (SPON) is a prominent and well-defined cell group of the superior olivary complex that sends significant but often neglected GABAergic projections to the IC. To investigate the trajectory, distribution and morphology of these projections, we injected the neuroanatomical tracer biotinylated dextran amine into the SPON of albino rats. Our results demonstrate that: (1) the SPON innervates densely all three subdivisions of the ipsilateral IC: central nucleus (CNIC), dorsal cortex (DCIC) and external cortex (ECIC). The SPON also sends a sparse projection to the contralateral DCIC via the commissure of the IC. (2) SPON axons are relatively thick (diameter >1.2 μm), ascend to the midbrain tectum in the medial aspect of the lateral lemniscus, and, for the most part, do not innervate the nuclei of the lateral lemniscus. (3) SPON fibers ramify profusely within the IC and bear abundant en passant and terminal boutons. (4) The axons of neurons in discrete regions of the SPON form two laminar terminal plexuses in the ipsilateral IC: a medial plexus that spans the CNIC and DCIC parallel to the known fibrodendritic laminae of the CNIC, and a lateral plexus located in the ECIC and oriented more or less parallel to the surface of the IC. (5) The projection from SPON to the ipsilateral IC is topographic: medial SPON neurons innervate the ventromedial region of the CNIC and DCIC and the ventrolateral region of the ECIC, whereas more laterally situated SPON neurons innervate more dorsolateral regions of the CNIC and DCIC and more dorsomedial regions of the ECIC. Thus, SPON fibers follow a pattern of distribution within the IC similar to that previously reported for intracollicular and corticocollicular projections.

Section snippets

Experimental procedures

Fifteen female Sprague–Dawley rats (body weight 190–210 g), obtained from the Animal Core Facility of the University of Salamanca, were cared for and used in compliance with the European Communities Council Directive of 24 November 1986 (86/609/EEC) regulations concerning the use of animals in biomedical research, and the experimental procedures were approved and supervised by the Animal Care and Use Committee of the University of Salamanca. For the surgical procedures, including the

Results

The information described herein comes from 15 selected experimental cases with single injections of BDA into the SPON of the albino rat. In 13 cases, the injection site was wholly contained within the limits of the nucleus (Fig. 1). In the remaining two cases, the injection site was located in the ventrolateral region of the SPON and encroached upon the neighboring medial superior olive (MSO). The locations of injection sites of various representative cases are illustrated schematically in

Technical considerations

The tracer used in this study, BDA, labels the axons of neurons at the injection site, but it is also known to label axons that innervate or cross the injection site, as well as their parent cell bodies. Consequently, BDA gives rise to so-called collateral transport, whereby the tracer taken up by a given axonal branch is transported retrogradely to a bifurcation in the axon, and then anterogradely into another branch (e.g. de Olmos and Heimer 1977, Merchán et al 1994, Warr et al 1997, Doucet

Acknowledgments

This work was supported by the Spanish Ministries of Education and Science and Innovation grants PB95-1129, BFI2000/1358, BFU2004-05909 and BFU2008-04197 (to E.S.), by the Junta de Castilla y León grants SA15/97, SA097/01, SA007C05 and GR221 (to E.S.), and by the National Institute on Deafness and Other Communication Disorders Grant RO 1 DC-02266 (to A.S.B.).

References (90)

  • A. Kadner et al.

    Encoding of temporal features of auditory stimuli in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat

    Neuroscience

    (2008)
  • J.B. Kelly et al.

    Projections from the superior olive and lateral lemniscus to tonotopic regions of the rat's inferior colliculus

    Hear Res

    (1998)
  • M. Kudo et al.

    Differential organization of crossed and uncrossed projections from the superior olive to the inferior colliculus in the mole

    Neurosci Lett

    (1990)
  • R.J. Kulesza

    Cytoarchitecture of the human superior olivary complex: nuclei of the trapezoid body and posterior tier

    Hear Res

    (2008)
  • R.J. Kulesza et al.

    Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat

    Hear Res

    (2002)
  • N. Kuwabara et al.

    Local collateral projections from the medial superior olive to the superior paraolivary nucleus in the gerbil

    Brain Res

    (1999)
  • A.F. Marshall et al.

    Auditory response properties of neurons in the tectal longitudinal column of the rat

    Hear Res

    (2008)
  • S. Okoyama et al.

    Postnatal development of the projection from the medial superior olive to the inferior colliculus in the rat

    Hear Res

    (1995)
  • R.L. Saint Marie et al.

    Neurotransmitter-specific uptake and retrograde transport of [3H]glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus

    Brain Res

    (1990)
  • R.L. Saint Marie et al.

    Spatial representation of frequency in the rat dorsal nucleus of the lateral lemniscus as revealed by acoustically induced c-fos mRNA expression

    Hear Res

    (1999)
  • M.E. Scheibel et al.

    Neuropil organization in the superior olive of the cat

    Exp Neurol

    (1974)
  • W.B. Warr et al.

    Efferent innervation of the inner hair cell region: origins and terminations of two lateral olivocochlear systems

    Hear Res

    (1997)
  • F.H. Willard et al.

    The auditory brainstem nuclei and some of their projections to the inferior colliculus in the North American opossum

    Neuroscience

    (1983)
  • F.H. Willard et al.

    Collateral innervation of the inferior colliculus in the North American opossum: a study using fluorescent markers in a double-labeling paradigm

    Brain Res

    (1984)
  • D.X. Zhang et al.

    GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat

    Hear Res

    (1998)
  • J.C. Adams

    Cytology of periolivary cells and the organization of their projections in the cat

    J Comp Neurol

    (1983)
  • A. Aschoff et al.

    Distribution of cochlear efferents and olivo-collicular neurons in the brainstem of rat and guinea pigA double labeling study with fluorescent tracers

    Exp Brain Res

    (1988)
  • M.I. Banks et al.

    Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body

    J Neurosci

    (1992)
  • O. Behrend et al.

    Auditory response properties in the superior paraolivary nucleus of the gerbil

    J Neurophysiol

    (2002)
  • J.K. Brunso-Bechtold et al.

    HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat

    J Comp Neurol

    (1981)
  • J.H. Casseday et al.

    Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus

    Science

    (1994)
  • J.R. Coleman et al.

    Sources of projections to subdivisions of the inferior colliculus in the rat

    J Comp Neurol

    (1987)
  • J.R. Doucet et al.

    Axonal pathways to the lateral superior olive labeled with biotinylated dextran amine injections in the dorsal cochlear nucleus of rats

    J Comp Neurol

    (2003)
  • R. Druga et al.

    Ascending and descending projections to the inferior colliculus of the rat

    Physiol Bohemoslov

    (1984)
  • H. Faye-Lund

    Projection from the inferior colliculus to the superior olivary complex in the albino rat

    Anat Embryol (Berl)

    (1986)
  • H. Faye-Lund et al.

    Anatomy of the inferior colliculus in rat

    Anat Embryol (Berl)

    (1985)
  • M. Feliciano et al.

    Direct projections from the rat primary auditory neocortex to nucleus sagulum, paralemniscal regions, superior olivary complex and cochlear nuclei

    Aud Neurosci

    (1995)
  • E. Friauf et al.

    Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase

    Exp Brain Res

    (1988)
  • R.D. Frisina et al.

    Functional organization of mustached bat inferior colliculus: IIConnections of the FM2 region

    J Comp Neurol

    (1989)
  • B.R. Glasberg et al.

    Psychoacoustic abilities of subjects with unilateral and bilateral cochlear hearing impairments and their relationship to the ability to understand speech

    Scand Audiol

    (1989)
  • K.K. Glendenning et al.

    Ascending auditory afferents to the nuclei of the lateral lemniscus

    J Comp Neurol

    (1981)
  • T. González-Hernández et al.

    Sources of GABAergic input to the inferior colliculus of the rat

    J Comp Neurol

    (1996)
  • B. Grothe et al.

    Anatomy and projection patterns of the superior olivary complex in the Mexican free-tailed bat, Tadarida brasiliensis mexicana

    J Comp Neurol

    (1994)
  • C.K. Henkel et al.

    Organization of the disynaptic pathway from the anteroventral cochlear nucleus to the lateral superior olivary nucleus in the ferret

    Anat Embryol (Berl)

    (1999)
  • O. Hernández et al.

    A GABAergic component in the commissure of the inferior colliculus in rat

    Neuroreport

    (2006)
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    Present address: Verónica Fuentes-Santamaría, Centro Regional de Investigaciones Biomédicas and Departamento de Ciencias Médicas, Facultad de Medicina, Universidad de Castilla-La Mancha, 02006-Albacete, Spain.

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