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Inhibitory and excitatory response areas of neurons in the central nucleus of the inferior colliculus in unanesthetized chinchillas

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Abstract

In unanesthetized chinchillas, we determined excitatory and inhibitory response regions of neurons in the central nucleus of the inferior colliculus (ICc). The responses of 250 multiunits and 47 single units in the ICc to one- and two-tone stimuli were measured by extracellular recordings. The one-tone excitatory response area of ICc neurons from awake chinchillas was classified as either narrow with a steep high-frequency slope >140 dB/oct (type 1), broad with a high-frequency slope <140 dB/oct (type 2), or complex with a negative high-frequency slope (type 3). One-tone inhibition was prominent only in units with a high spontaneous firing rate. As revealed with two-tone stimuli, inhibition in the ICc of awake chinchillas and its relation to excitatory response regions was different from what is reported in anesthetized animals. The two-tone inhibitory responses were classified as follows: (1) inhibitory regions of equal strength on both sides of the characteristic frequency; (2) asymmetrical inhibitory regions, more prominent at the high-frequency side of the characteristic frequency; (3) strong inhibitory regions overlying most of the one-tone excitatory response region; (4) inhibitory response regions lying only within the one-tone excitatory response region; and (5) neurons without clear two-tone inhibition. One-tone and two-tone inhibitory regions of the same unit were markedly different in 66% of the units with a high spontaneous rate. The neural response to frequencies within the inhibitory regions often was an onset response followed by inhibition. Excitatory and inhibitory response properties were similar over considerable penetration distances (600–1,000 μm) in a particular dorso-ventral recording track.

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References

  • Abeles M, Goldstein MH Jr (1972) Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs. Brain Res 42:337–352

    Article  PubMed  CAS  Google Scholar 

  • Amin J (1999) A single hydrophobic residue confers barbiturate sensitivity to gamma-aminobutyric acid type C receptor. Mol Pharmacol 55:411–423

    PubMed  CAS  Google Scholar 

  • Antkowiak B (2001) How do general anaesthetics work? Naturwissenschaften 88:201–213

    Article  PubMed  CAS  Google Scholar 

  • Astl J, Popelar J, Kvasnak E, Syka J (1996) Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. Audiology 35:335–345

    Article  PubMed  CAS  Google Scholar 

  • Belelli D, Lambert JJ, Peters JA, Wafford K, Whiting PJ (1997) The interaction of the general anesthetic etomidate with the gamma-aminobutyric acid type A receptor is influenced by a single amino acid. Proc Natl Acad Sci USA 94:11031–11036

    Article  PubMed  CAS  Google Scholar 

  • Biebel UW, Langner G (2002) Evidence for interactions across frequency channels in the inferior colliculus of awake chinchilla. Hear Res 169:151–168

    Article  PubMed  Google Scholar 

  • Bock GR, Webster WR, Aitkin LM (1972) Discharge patterns of single units in inferior colliculus of the alert cat. J Neurophysiol 35:265–277

    PubMed  CAS  Google Scholar 

  • Brown M, Webster WR, Martin RL (1997) The three-dimensional frequency organization of the inferior colliculus of the cat: a 2-deoxyglucose study. Hear Res 104:57–72

    Article  PubMed  CAS  Google Scholar 

  • Caird DM, Klinke R (1983) Processing of binaural stimuli by cat superior olivary complex neurons. Exp Brain Res 52:385–399

    Article  PubMed  CAS  Google Scholar 

  • Caspary DM, Palombi PS, Hughes LF (2002) GABAergic inputs shape responses to amplitude modulated stimuli in the inferior colliculus. Hear Res 168:163–173

    Article  PubMed  CAS  Google Scholar 

  • Davis KA (2002) Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus. J Neurophysiol 87:1824–1835

    PubMed  Google Scholar 

  • Davis KA, Young ED (2000) Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J Neurophysiol 83:926–940

    PubMed  CAS  Google Scholar 

  • Davis KA, Ramachandran R, May BJ (1999) Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. J Neurophysiol 82:164–175

    PubMed  CAS  Google Scholar 

  • Egorova M, Ehret G, Vartanian I, Esser KH (2001) Frequency response areas of neurons in the mouse inferior colliculus. I. Threshold and tuning characteristics. Exp Brain Res 140:145–161

    Article  PubMed  CAS  Google Scholar 

  • Ehret G (1997) The auditory midbrain, a “shunting yard” of acoustical information processing. In: Ehret G, Romand R (eds) The central auditory system. Oxford University Press, Oxford, pp 259–316

    Google Scholar 

  • Ehret G, Merzenich MM (1988a) Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat. Brain Res 472:139–163

    CAS  Google Scholar 

  • Ehret G, Merzenich MM (1988b) Neuronal discharge rate is unsuitable for encoding sound intensity at the inferior-colliculus level. Hear Res 35:1–8

    Article  CAS  Google Scholar 

  • Ehret G, Egorova M, Hage SR, Muller BA (2003) Spatial map of frequency tuning-curve shapes in the mouse inferior colliculus. Neuroreport 14:1365–1369

    Article  PubMed  Google Scholar 

  • Evans EF, Zhao W (1993) Varieties of inhibition in the processing and control of processing in the mammalian cochlear nucleus. Prog Brain Res 97:117–126

    Article  PubMed  CAS  Google Scholar 

  • Faingold CL, Anderson CA (1991) Loss of intensity-induced inhibition in inferior colliculus neurons leads to audiogenic seizure susceptibility in behaving genetically epilepsy-prone rats. Exp Neurol 113:354–363

    Article  PubMed  CAS  Google Scholar 

  • Fubara BM, Casseday JH, Covey E, Schwartz-Bloom RD (1996) Distribution of GABA(A), GABA(B), and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus. J Comp Neurol 369:83–92

    Article  PubMed  CAS  Google Scholar 

  • Funkenstein HH, Winter P (1973) Responses to acoustic stimuli of units in the auditory cortex of awake squirrel monkeys. Exp Brain Res 18:464–488

    Article  PubMed  CAS  Google Scholar 

  • Fuzessery ZM, Hall JC (1996) Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol 76:1059–1073

    PubMed  CAS  Google Scholar 

  • Gaese BH, Ostwald J (2001) Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex. J Neurophysiol 86:1062–1066

    PubMed  CAS  Google Scholar 

  • Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613–636

    PubMed  CAS  Google Scholar 

  • Goldstein MH Jr, Abeles M (1975) Note on tonotopic organization of primary auditory cortex in the cat. Brain Res 100:188–191

    Article  PubMed  Google Scholar 

  • Hage SR, Ehret G (2003) Mapping responses to frequency sweeps and tones in the inferior colliculus of house mice. Eur J Neurosci 18:2301–2312

    Article  PubMed  Google Scholar 

  • Hernández O, Espinosa N, Pérez-González D, Malmierca MS (2005) The inferior colliculus of the rat: a quantitative analysis of monaural frequency response areas. Neuroscience 132:203–217

    Article  PubMed  CAS  Google Scholar 

  • Hill KG, Geisler CD (1992) Two-tone suppression, excitation and the after effect in rate responses in auditory nerve fibres in the cat. Hear Res 64:52–60

    Article  PubMed  CAS  Google Scholar 

  • Kiang NY (1968) A survey of recent developments in the study of auditory physiology. Ann Otol Rhinol Laryngol 77:656–675

    PubMed  CAS  Google Scholar 

  • Kiang NYS, Watanbe T, Thomas EC, Clark LF (1965) Discharge patterns of single fibers in the cat’s auditory nerve. MIT Press, Cambridge

    Google Scholar 

  • Koch U, Grothe B (1998) GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol 80:71–82

    PubMed  CAS  Google Scholar 

  • Kopp-Scheinpflug C (1999) Interaktion von Exzitation und Inhibition bei der zentralnervösen Verarbeitung akustischer Information. Universität Leibzig

  • Kuwada S, Batra R, Yin TC, Oliver DL, Haberly LB, Stanford TR (1997) Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci 17:7565–7581

    PubMed  CAS  Google Scholar 

  • Langner G, Schreiner CE (1988) Periodicity coding in the inferior colliculus of the cat. I. neuronal mechanisms. J Neurophysiol 60:1799–1822

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455

    Article  PubMed  CAS  Google Scholar 

  • Loftus WC, Bishop DC, Saint Marie RL, Oliver DL (2004) Organization of binaural excitatory and inhibitory inputs to the inferior colliculus from the superior olive. J Comp Neurol 472:330–344

    Article  PubMed  Google Scholar 

  • Malmierca MS, Rees A, Le Beau FEN, 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

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • McAlpine D, Palmer AR (2002) Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J Neurosci 22:1443–1453

    PubMed  CAS  Google Scholar 

  • McAlpine D, Jiang D, Palmer AR (1996) Interaural delay sensitivity and the classification of low best-frequency binaural responses in the inferior colliculus of the guinea pig. Hear Res 97:136–152

    Article  PubMed  CAS  Google Scholar 

  • Merzenich MM, Reid MD (1974) Representation of the cochlea within the inferior colliculus of the cat. Brain Res 77:397–415

    Article  PubMed  CAS  Google Scholar 

  • Möller J (1978) Response characteristics of inferior colliculus neurons of awake cf-fm bat rhinolophus ferrumequinum-2. Two-tone stimulation. J Comp Physiol 125:227–236

    Article  Google Scholar 

  • Nagai T, Maeda T, Imai H, McGeer PL, McGeer EG (1985) Distribution of GABA-T-intensive neurons in the rat hindbrain. J Comp Neurol 231:260–269

    Article  PubMed  CAS  Google Scholar 

  • Oliver DL, Huerta MF (1992) Inferior and superior colliculi. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway, vol 1. Springer, Berlin Heidelberg New York, pp 168–221

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Oliver DL, Winer JA, Beckius GE, Saint Marie RL (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J Comp Neurol 340:27–42

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Palombi PS, Caspary DM (1996b) Responses of young and aged Fischer 344 rat inferior colliculus neurons to binaural tonal stimuli. Hear Res 100:59–67

    Article  CAS  Google Scholar 

  • Park TJ, Pollak GD (1994) Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat. J Neurophysiol 72:1080–1102

    PubMed  CAS  Google Scholar 

  • Pedemonte M, Torterolo P, Velluti RA (1997) In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs. Brain Res 759:24–31

    Article  PubMed  CAS  Google Scholar 

  • Pelleg-Toiba R, Wollberg Z (1989) Tuning properties of auditory cortex cells in the awake squirrel monkey. Exp Brain Res 74:353–364

    Article  PubMed  CAS  Google Scholar 

  • Pollak GD, Park TJ (1993) The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat’s inferior colliculus. Hear Res 65:99–117

    Article  PubMed  CAS  Google Scholar 

  • Ramachandran R, Davis KA, May BJ (1999) Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J Neurophysiol 82:152–163

    PubMed  CAS  Google Scholar 

  • Reetz G, Ehret G (1999) Inputs from three brainstem sources to identified neurons of the mouse inferior colliculus. Brain Res 816:527–543

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Romand R, Avan P (1997) Anatomical and functional aspects of the cochlear nucleus. In: Ehret G, Romand R (eds) The central auditory system. Oxford University Press, Oxford, pp 97–191

    Google Scholar 

  • Sachs MB, Kiang NY (1968) Two-tone inhibition in auditory-nerve fibers. J Acoust Soc Am 43:1120–1128

    Article  PubMed  CAS  Google Scholar 

  • Saint Marie RL, Morest DK, Brandon CJ (1989a) 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sanes DH, Malone BJ, Semple MN (1998) Role of synaptic inhibition in processing of dynamic binaural level stimuli. J Neurosci 18:794–803

    PubMed  CAS  Google Scholar 

  • Scheich H, Bonke BA, Bonke D, Langner G (1979) Functional organization of some auditory nuclei in the guinea fowl demonstrated by the 2-deoxyglucose technique. Cell Tissue Res 204:17–27

    Article  PubMed  CAS  Google Scholar 

  • Schmiedt RA (1982) Boundaries of two-tone rate suppression of cochlear-nerve activity. Hear Res 7:335–351

    Article  PubMed  CAS  Google Scholar 

  • Semple MN, Aitkin LM (1979) Representation of sound frequency and laterality by units in central nucleus of cat inferior colliculus. J Neurophysiol 42(6):1626–1639

    PubMed  CAS  Google Scholar 

  • Servière J, Webster WR, Calford MB (1984) Isofrequency labelling revealed by a combined [4c]-2-deoxyglucose, electrophysiological, and horseradish peroxidase study of the inferior colliculus of the cat. J Comp Neurol 228:463–477

    Article  PubMed  Google Scholar 

  • Shneiderman A, Oliver DL (1989) EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: a possible source of inhibitory inputs to the inferior colliculus. J Comp Neurol 286:28–47

    Article  PubMed  CAS  Google Scholar 

  • Spirou GA, Young ED (1991) Organization of dorsal cochlear nucleus type-IV unit response maps and their relationship to activation by bandlimited noise. J Neurophysiol 66:1750–1768

    PubMed  CAS  Google Scholar 

  • Stiebler I (1986) Tone threshold mapping in the inferior colliculus of the house mouse. Neurosci Lett 65:336–340

    Article  PubMed  CAS  Google Scholar 

  • Suga N (1969) Classification of inferior collicular neurones of bats in terms of responses to pure tones, FM sounds and noise bursts. J Physiol 200:555–574

    PubMed  CAS  Google Scholar 

  • Tan AY, Zhang LI, Merzenich MM, Schreiner CE (2004) Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92:630–643

    Article  PubMed  Google Scholar 

  • Thompson AM (2005) Descending connections of the auditory midbrain. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, Berlin Heidelberg New York, pp 182–199

    Chapter  Google Scholar 

  • Thompson GC, Cortez AM, Lam M-K (1985) Localization of GABA immunoreactivity in the auditory brainstem of guinea pigs. Brain Res 339:119–122

    Article  PubMed  CAS  Google Scholar 

  • Vaughn MD, Pozza MF, Lingenhohl K (1996) Excitatory acoustic responses in the inferior colliculus of the rat are increased by GABAB receptor blockade. Neuropharmacology 35:1761–1767

    Article  PubMed  CAS  Google Scholar 

  • Wagner T (1994) Intrinsic properties of identified neurons in the central nucleus of mouse inferior colliculus. Neuroreport 6:89–93

    Article  PubMed  CAS  Google Scholar 

  • Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–446

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson L (2004) Classification and regression trees. SYSTAT11 Statistics I. SYSTAT software, Inc., Richmond, pp 35–56

    Google Scholar 

  • Winer JA, Schreiner CE (2005) The central auditory system. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer Berlin Heidelberg New York, pp 1–68

    Chapter  Google Scholar 

  • Winer JA, Larue DT, Pollak GD (1995) GABA and glycine in the central auditory system of the mustache bat: structural substrates for inhibitory neuronal organization. J Comp Neurol 355:317–353

    Article  PubMed  CAS  Google Scholar 

  • Wu SH, Ma CL, Kelly JB (2004) Contribution of AMPA, NMDA, and GABA(A) receptors to temporal pattern of postsynaptic responses in the inferior colliculus of the rat. J Neurosci 24:4625–4634

    Article  PubMed  CAS  Google Scholar 

  • Yamamura T, Harada K, Okamura A, Kemmotsu O (1990) Is the site of action of ketamine anesthesia the N-methyl-d-aspartate receptor? Anesthesiology 72:704–710

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Suga N (1996) The midbrain creates and the thalamus sharpens echo-delay tuning for the cortical representation of target-distance information in the mustached bat. Hear Res 93:102–110

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Zhang Y, Ehret G (2005) Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. J Neurophysiol 93:71–83

    Article  PubMed  Google Scholar 

  • Zhang Y, Wu SH (2000) Long-term potentiation in the inferior colliculus studied in rat brain slice. Hear Res 147:92–103

    Article  PubMed  CAS  Google Scholar 

  • Zurita P, Villa AE, de Ribaupierre Y, de Ribaupierre F, Rouiller EM (1994) Changes of single unit activity in the cat’s auditory thalamus and cortex associated to different anesthetic conditions. Neurosci Res 19:303–316

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors thank Rainer Klinke and Marcus Müller for thoughtful reading of and comments on earlier versions of this manuscript. We also acknowledge Désirée Biedenkapp’s participation in many of the experiments. This work was supported by the Deutsche Forschungsgemeinschaft (SFB 269-B1 and by a grant of the graduate college GRK 361).

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  1. Physiologisches Institut II, Theodor-Stern Kai 7, 60590, Frankfurt/Main, Germany

    Ala Alkhatib, Ulrich W. Biebel & Jean W. T. Smolders

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  1. Ala Alkhatib
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Alkhatib, A., Biebel, U.W. & Smolders, J.W.T. Inhibitory and excitatory response areas of neurons in the central nucleus of the inferior colliculus in unanesthetized chinchillas. Exp Brain Res 174, 124–143 (2006). https://doi.org/10.1007/s00221-006-0424-8

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