Skip to main content
SpringerLink
Log in

The commissure of the inferior colliculus shapes frequency response areas in rat: an in vivo study using reversible blockade with microinjection of kynurenic acid

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The commissure of the inferior colliculus (CoIC) interconnects corresponding frequency-band laminae in the two inferior colliculi (ICs). Although the CoIC has been studied neurophysiologically in vitro, the effect of the CoIC on the responses of IC neurons to physiological stimuli has not been addressed. In this study, we injected the glutamate receptor blocker kynurenic acid into one IC while recording the frequency response areas (FRAs) of neurons in the other, to test the hypothesis that frequency response properties of IC neurons are influenced by commissural inputs from the contralateral IC. Following blockade of the commissure, 10 of 12 neurons tested exhibited an increase or a decrease in their FRAs. In most neurons (9/12) the response area changed in the same direction, irrespective of whether the neuron was stimulated monaurally (at the ear contralateral to the recorded IC) or binaurally. In one neuron, blockade of the CoIC resulted in an expansion of the response area under binaural stimulation and a contraction under monaural stimulation. In the remaining two units, no effect was observed. Changes in response areas that exceeded the criterion ranged between 17 and 80% of control values with monaural stimulation, and 35 and 77% with binaural stimulation. Area changes could also be accompanied by changes in spike rate and monotonicity. From our observation that FRAs contract following commissure block, we infer that the commissure contains excitatory fibres. The expansion of response areas in other cases, however, suggests that the commissure also contains inhibitory fibres, or that its effects are mediated by disynaptic as well as monosynaptic circuits. The small sample size precludes a definitive conclusion as to which effect predominates. We conclude that inputs from the contralateral IC projecting via the CoIC influence the spectral selectivity and response gain of neurons in the IC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A–C.
Fig. 2A–D.
Fig. 3A–D.
Fig. 4A–D.

Similar content being viewed by others

References

  • Burger RM, Pollak GD (2001) Reversible inactivation of the dorsal nucleus of the lateral lemniscus reveals its role in the processing of multiple sound sources in the inferior colliculus of bats. J Neurosci 21:4830–4843

    CAS  PubMed  Google Scholar 

  • Chernock ML, Winer JA (2001) Organization of bilateral projections from the inferior colliculus to the medial geniculate body. Soc Neurosci Abstr. 27:930.10

    Google Scholar 

  • Coleman JR, Clerici WJ (1987) Sources of projections to subdivisions of the inferior colliculus in the rat. J Comp Neurol 262:215–226

    CAS  PubMed  Google Scholar 

  • Evans EF (1979) Single unit studies of the mammalian auditory nerve. In: Beagley HA (ed) Auditory investigations: the scientific and technological basis. Oxford University Press, Oxford, pp 324–367

  • Faingold CL, Hoffmann WE, Caspary DM (1989) Effects of excitant amino acids on acoustic responses of inferior colliculus neurons. Hear Res 40:127–136

    CAS  PubMed  Google Scholar 

  • Foeller E, Vater M, Kössl M (2001) Laminar analysis of inhibition in the gerbil primary auditory cortex. J Assoc Res Otolaryngol 2:279–296

    CAS  PubMed  Google Scholar 

  • González-Hernández T, Mantolán-Sarmiento B, González-González B, Pérez-González H (1996) Sources of GABAergic input to the inferior colliculus of the rat. J Comp Neurol 372:309–326

    PubMed  Google Scholar 

  • Henkel CK, Spangler KM (1983) Organization of the efferent projections of the medial superior olivary nucleus in the cat as revealed by HRP and autoradiographic tracing methods. J Comp Neurol 221:416–428

    CAS  PubMed  Google Scholar 

  • Kelly JB, Kavanagh GL (1994) Sound localization after unilateral lesions of inferior colliculus in the ferret (Mustela putorius). J Neurophysiol 71:1078–1087

    CAS  PubMed  Google Scholar 

  • Kelly JB, Zhang H (2002) Contribution of AMPA and NMDA receptors to excitatory responses in the inferior colliculus. Hear Res 168:35–42

    Article  CAS  PubMed  Google Scholar 

  • Le Beau FE, Rees A, Malmierca MS (1996) The contribution of GABA and glycine mediated inhibition to the monoaural temporal response properties of neurons in the inferior colliculus. J Neurophysiol 75:902–919

    PubMed  Google Scholar 

  • LeBeau FE, Malmierca MS, Rees A (2001) Iontophoresis in vivo demonstrates a key role for GABAA and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21:7303–7312

    CAS  PubMed  Google Scholar 

  • Li L, Kelly JB (1992) Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus. J Neurosci 12:4530–4539

    CAS  PubMed  Google Scholar 

  • Ma CL, Kelly JB, Wu SH (2002) AMPA and NMDA receptors mediate synaptic excitation in the rat's inferior colliculus. Hear Res 168:25–34

    Article  CAS  PubMed  Google Scholar 

  • Malmierca MS, Merchán MA (2003) Auditors system. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego (in press)

  • Malmierca MS, Blackstad TW, Osen KK, Karagülle T, Molowny RL (1993) The central nucleus of the inferior colliculus in rat, A Golgi and Computer reconstruction study of neuronal and laminar structure. J Comp Neurol 333:1–27

    CAS  PubMed  Google Scholar 

  • Malmierca MS, Rees A, Le Beau FE, Bjaalie JG (1995) Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357:124–144

    CAS  PubMed  Google Scholar 

  • Malmierca MS, Merchán MA, Oliver DL (1999) Convergence of dorsal and ventral cochlear nuclei input onto frequency-band laminae of the inferior colliculus, a double tracer study in rat and cat. ARO Abstracts 22:221

    Google Scholar 

  • Malmierca MS, Hernández O, Falconi A, Merchán MA, Rees A (2001) The commissure of the inferior colliculus: anatomical and physiological correlates. ARO Abstracts 24:635

    Google Scholar 

  • Malmierca MS, Hernández O, Falconi A, Merchán MA, Rees A (2002a) Functional mechanisms mediated by the commissure of the inferior colliculus. Central auditory processing. Proceedings Monte Veritá, Ascona, Switzerland, p 53

  • Malmierca MS, Merchán MA, Henkel CH, Oliver DL (2002b) Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci 22:10891–10897

    CAS  PubMed  Google Scholar 

  • Moore DR, Kotak VC, Sanes DH (1998) Commissural and lemniscal synaptic input to the gerbil inferior colliculus. J Neurophysiol 80:2229–2236

    CAS  PubMed  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 (1987) Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat, possible substrates for binaural interaction. J Comp Neurol 264:24–46

    CAS  PubMed  Google Scholar 

  • Oliver DL, Kuwada S, Yin TC, Haberly LB, Henkel CK (1991) Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J Comp Neurol 303:75–100

    CAS  PubMed  Google Scholar 

  • Osen KK (1972) Projections of the cochlear nuclei in the cat. J Comp Neurol 136:453–484

    Google Scholar 

  • Palombi PS, Caspary DM (1996) GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons. J Neurophysiol 75:2211–2219

    CAS  PubMed  Google Scholar 

  • Rees A, Sarbaz A, Malmierca MS, Le Beau FE (1997) Regularity of firing of neurons in the inferior colliculus. J Neurophysiol 77:2945–2965

    CAS  PubMed  Google Scholar 

  • Riquelme R, Saldaña E, Osen KK, Ottersen OP, Merchán MA (2001) Colocalization of GABA and Glycine in the ventral nucleus of the lateral lemniscus in rat, an in situ hybridization and semiquantitative inmunocytochemical study. J Comp Neurol 432:409–424

    Article  CAS  PubMed  Google Scholar 

  • Saint Marie RL (1996) Glutamatergic connections of the auditory midbrain: selective uptake and axonal transport of d-[3H]aspartate. J Comp Neurol 373:255–270

    Article  PubMed  Google Scholar 

  • Saint Marie RL, Ostapoff DK, Morest DK, Wenthold RJ (1989) Glycine-inmunoreactive projection of the cat lateral superior olive, possible role in mibrain ear dominance. J Comp Neurol 279:382–396

    PubMed  Google Scholar 

  • Saldaña E, Merchán MA (1992) Intrinsic and commissural connections of the rat inferior colliculus. J Comp Neurol 319:417–437

    PubMed  Google Scholar 

  • Smith PH (1992) Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique. J Neurosci 12:3700–3715

    CAS  PubMed  Google Scholar 

  • Yang L, Pollak GD, Resler C (1992) GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol 68:1760–1774

    CAS  PubMed  Google Scholar 

  • Zhang H, Kelly JB (2001) AMPA and NMDA receptors regulate responses of neurons in the rat's inferior colliculus. J Neurophysiol 86:871–880

    CAS  PubMed  Google Scholar 

  • Zhang DX, Li L, Kelly JB, Wu SH (1998) GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat. Hear Res 117:1–12

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Jack Kelly and Brian Van Adel for advice on the pressure injection technique. This study was supported by grants from the Spanish DGES (BFI-2000-1396) and JCYL-UE (SA084/01) (MSM, MAM), and The Wellcome Trust (066348) (AR, MSM, MAM). OH held a fellowship from the Spanish MCYT (FP-2000-5811 and BFI 2000/1358) and AF a fellowship from the Spanish AECI.

Author information

Authors and Affiliations

  1. Laboratory for the Neurobiology of Hearing, Institute for Neuroscience of Castilla y León and Faculty of Medicine, University of Salamanca, Salamanca, Spain

    Manuel S. Malmierca, Olga Hernández, Atilio Falconi, Enrique A. Lopez-Poveda & Miguel Merchán

  2. School of Neurology, Neurobiology and Psychiatry, The Medical School, University of Newcastle upon Tyne, Newcastle upon Tyne, NE2 4HH, UK

    Adrian Rees

Authors
  1. Manuel S. Malmierca
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olga Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atilio Falconi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Enrique A. Lopez-Poveda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miguel Merchán
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Adrian Rees
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel S. Malmierca.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Malmierca, M.S., Hernández, O., Falconi, A. et al. The commissure of the inferior colliculus shapes frequency response areas in rat: an in vivo study using reversible blockade with microinjection of kynurenic acid. Exp Brain Res 153, 522–529 (2003). https://doi.org/10.1007/s00221-003-1615-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-003-1615-1

Keywords

Search

Navigation