The superior paraolivary nucleus shapes temporal response properties of neurons in the inferior colliculus

Abstract

The mammalian superior paraolivary nucleus (SPON) is a major source of GABAergic inhibition to neurons in the inferior colliculus (IC), a well-studied midbrain nucleus that is the site of convergence and integration for the majority ascending auditory pathways en route to the cortex. Neurons in the SPON and IC exhibit highly precise responses to temporal sound features, which are important perceptual cues for naturally occurring sounds. To determine how inhibitory input from the SPON contributes to the encoding of temporal information in the IC, a reversible inactivation procedure was conducted to silence SPON neurons, while recording responses to amplitude-modulated tones and silent gaps between tones in the IC. The results show that SPON-derived inhibition shapes responses of onset and sustained units in the IC via different mechanisms. Onset neurons appear to be driven primarily by excitatory inputs and their responses are shaped indirectly by SPON-derived inhibition, whereas sustained neurons are heavily influenced directly by transient offset inhibition from the SPON. The findings also demonstrate that a more complete dissection of temporal processing pathways is critical for understanding how biologically important sounds are encoded by the brain.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Allen PD, Burkard RF, Ison JR, Walton JP (2003) Impaired gap encoding in aged mouse inferior colliculus at moderate but not high stimulus levels. Hear Res 186:17–29

    Article  PubMed  Google Scholar 

  2. Anderson S, Parbery-Clark A, White-Schwoch T, Drehobl S, Kraus N (2013) Effects of hearing loss on the subcortical representation of speech cues. J Acoust Soc Am 133:3030–3038

    PubMed Central  Article  PubMed  Google Scholar 

  3. Barsz K, Ison JR, Snell KB, Walton JP (2002) Behavioral and neural measures of auditory temporal acuity in aging humans and mice. Neurobiol Aging 23:565–578

    Article  PubMed  Google Scholar 

  4. Batschelet E (1981) Circular statistics in biology. Academic Press, London

    Google Scholar 

  5. Bauer EE, Klug A, Pollak GD (2000) Features of contralaterally evoked inhibition in the inferior colliculus. Hear Res 141:80–96

    CAS  Article  PubMed  Google Scholar 

  6. Baumann S, Griffiths TD, Rees A, Hunter D, Sun L, Thiele A (2010) Characterization of the BOLD response time course at different levels of the auditory pathway in non-human primates. Neuroimage 50:1099–1108

    PubMed Central  Article  PubMed  Google Scholar 

  7. Behrend O, Brand A, Kapfer C, Grothe B (2002) Auditory response properties in the superior paraolivary nucleus of the gerbil. J Neurophysiol 87:2915–2928

    PubMed  Google Scholar 

  8. Burger RM, Pollak GD (1998) Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus. J Neurophysiol 80:1686–1701

    CAS  PubMed  Google Scholar 

  9. 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 

  10. Cangiano L, Gargini C, Della Santina L, Demontis GC, Cervetto L (2007) High-pass filtering of input signals by the Ih current in a non-spiking neuron, the retinal rod bipolar cell. PLoS One 2:e1327

    PubMed Central  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  13. Dehmel S, Kopp-Scheinpflug C, Dorrscheidt GJ, Rubsamen R (2002) Electrophysiological characterization of the superior paraolivary nucleus in the Mongolian gerbil. Hear Res 172:18–36

    Article  PubMed  Google Scholar 

  14. Drullman R (1995) Temporal envelope and fine structure cues for speech intelligibility. J Acoust Soc Am 97:585–592

    CAS  Article  PubMed  Google Scholar 

  15. Faingold CL, Travis MA, Gehlbach G, Hoffmann WE, Jobe PC, Laird HE, Caspary DM (1986) Neuronal response abnormalities in the inferior colliculus of the genetically epilepsy-prone rat. Electroencephalogr Clin Neurophysiol 63:296–305

    CAS  Article  PubMed  Google Scholar 

  16. Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol (Berl) 175:35–52

    CAS  Article  Google Scholar 

  17. Felix RA, Fridberger A, Leijon S, Berrebi AS, Magnusson AK (2011) Sound rhythms are encoded by post-inhibitory rebound spiking in the superior paraolivary nucleus. J Neurosci 31:12566–12578

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  18. Felix RA, Kadner A, Berrebi AS (2012) Effects of ketamine on response properties of neurons in the superior paraolivary nucleus of the mouse. Neuroscience 201:307–319

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  19. Frisina RD (2001) Subcortical neural coding mechanisms for auditory temporal processing. Hear Res 158:1–27

    CAS  Article  PubMed  Google Scholar 

  20. Gittelman JX, Wang L, Colburn HS, Pollak GD (2012) Inhibition shapes response selectivity in the inferior colliculus by gain modulation. Front Neural Circuits 18(6):67

    Google Scholar 

  21. 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

    CAS  PubMed  Google Scholar 

  22. Grothe B (1994) Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. J Neurophysiol 71:706–721

    CAS  PubMed  Google Scholar 

  23. Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012

    CAS  Article  PubMed  Google Scholar 

  24. Havey DC, Caspary DM (1980) A simple technique for constructing “piggyback” multibarrel microelectrodes. Electroencephalogr Clin Neurophysiol 48:249–251

    CAS  Article  PubMed  Google Scholar 

  25. Henry KS, Heinz MG (2012) Diminished temporal coding with sensorineural hearing loss emerges in background noise. Nat Neurosci 15:1362–1364

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  26. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577

    CAS  Article  PubMed  Google Scholar 

  27. Kadner A, Berrebi AS (2008) Encoding of temporal features of auditory stimuli in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat. Neuroscience 151:868–887

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  28. Kadner A, Kulesza RJ, Berrebi AS (2006) Neurons in the medial nucleus of the trapezoid body and superior paraolivary nucleus of the rat may play a role in sound duration coding. J Neurophysiol 95:1499–1508

    Article  PubMed  Google Scholar 

  29. Kelly JB, Masterton B (1977) Auditory sensitivity of the albino rat. J Comp Physiol Psychol 91:930–936

    CAS  Article  PubMed  Google Scholar 

  30. Kelly JB, Liscum A, van Adel B, Ito M (1998) Projections from the superior olive and lateral lemniscus to tonotopic regions of the rat’s inferior colliculus. Hear Res 116:43–54

    CAS  Article  PubMed  Google Scholar 

  31. Klug A, Bauer EE, Pollak GD (1999) Multiple components of ipsilaterally evoked inhibition in the inferior colliculus. J Neurophysiol 82:593–610

    CAS  PubMed  Google Scholar 

  32. Koch and Grothe (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  Google Scholar 

  33. Koch U, Grothe B (2003) Hyperpolarization-activated current (Ih) in the inferior colliculus: distribution and contribution to temporal processing. J Neurophysiol 90:3679–3687

    Article  PubMed  Google Scholar 

  34. Kopp-Scheinpflug C, Tozer AJ, Robinson SW, Tempel BL, Hennig MH, Forsythe ID (2011) The sound of silence: ionic mechanisms encoding sound termination. Neuron 71:911–925

    CAS  Article  PubMed  Google Scholar 

  35. Krishna BS, Semple MN (2000) Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J Neurophysiol 84:255–273

    CAS  PubMed  Google Scholar 

  36. Kulesza RJ, Berrebi AS (2000) Superior paraolivary nucleus of the rat is a GABAergic nucleus. J Assoc Res Otolaryngol 1:255–269

    PubMed Central  Article  PubMed  Google Scholar 

  37. Kulesza RJ, Spirou GA, Berrebi AS (2003) Physiological response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 89:2299–2312

    Article  PubMed  Google Scholar 

  38. Kulesza RJ, Kadner A, Berrebi AS (2007) Distinct roles for glycine and GABA in shaping the response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 97:1610–1620

    CAS  Article  PubMed  Google Scholar 

  39. Kuwada S, Batra R (1999) Coding of sound envelopes by inhibitory rebound in neurons of the superior olivary complex in the unanesthetized rabbit. J Neurosci 19:2273–2287

    CAS  PubMed  Google Scholar 

  40. Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115–142

    CAS  Article  PubMed  Google Scholar 

  41. Lumani A, Zhang H (2010) Responses of neurons in the rat’s dorsal cortex of the inferior colliculus to monaural tone bursts. Brain Res 1351:115–129

    CAS  Article  PubMed  Google Scholar 

  42. Malmierca MS, Hernandez O, Antunes FM, Rees A (2009) Divergent and point-to-point connections in the commissural pathway between the inferior colliculi. J Comp Neurol 514:226–239

    PubMed Central  Article  PubMed  Google Scholar 

  43. Oliver DL, Morest DK (1984) The central nucleus of the inferior colliculus of the cat. J Comp Neurol 222:237–264

    CAS  Article  PubMed  Google Scholar 

  44. 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  PubMed  Google Scholar 

  45. Palombi PS, Caspary DM (1996b) Physiology of the young adult Fischer 344 rat inferior colliculus: responses to contralateral monaural stimuli. Hear Res 100:41–58

    CAS  Article  PubMed  Google Scholar 

  46. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, San Diego

    Google Scholar 

  47. Pollak GD (2013) The dominant role of inhibition in creating response selectivities for communication calls in the brainstem auditory system. Hear Res. doi:10.1016/j.heares.2013.03.001

    PubMed Central  PubMed  Google Scholar 

  48. Pollak GD, Gittelman JX, Li N, Xie R (2011) Inhibitory projections from the ventral nucleus of the lateral lemniscus and superior paraolivary nucleus create directional selectivity of frequency modulations in the inferior colliculus: a comparison of bats with other mammals. Hear Res 273:134–144

    PubMed Central  Article  PubMed  Google Scholar 

  49. Portfors CV, Felix RA (2005) Spectral integration in the inferior colliculus of the CBA/CaJ mouse. Neuroscience 136:1159–1170

    CAS  Article  PubMed  Google Scholar 

  50. Saldaña E, Berrebi AS (2000) Anisotropic organization of the rat superior paraolivary nucleus. Anat Embryol (Berl) 202:265–279

    Article  Google Scholar 

  51. Saldaña E, Merchan MA (2005) Intrinsic and commissural connections of the inferior colliculus. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York

    Google Scholar 

  52. Saldaña E, Aparicio MA, Fuentes-Santamaria V, Berrebi AS (2009) Connections of the superior paraolivary nucleus of the rat: projections to the inferior colliculus. Neuroscience 163:372–387

    PubMed Central  Article  PubMed  Google Scholar 

  53. Shamma SA, Micheyl C (2010) Behind the scenes of auditory perception. Curr Opin Neurobiol 20:361–366

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  54. Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primary temporal cues. Science 270:303–304

    CAS  Article  PubMed  Google Scholar 

  55. Sivaramkrishnan S, Oliver DL (2001) Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. J Neurosci 21:2861–2877

    Google Scholar 

  56. Sun H, Wu SH (2008) Physiological characteristics of postinhibitory rebound depolarization in neurons of the rat’s dorsal cortex of the inferior colliculus studies in vitro. Brain Res 1226:70–81

    CAS  Article  PubMed  Google Scholar 

  57. Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127–143

    Article  PubMed  Google Scholar 

  58. Walton JP, Frisina RD, Ison JR, O’Neill WE (1997) Neural correlates of behavioral gap detection in the inferior colliculus of the young CBA mouse. J Comp Physiol [A] 181:161–176

    CAS  Article  Google Scholar 

  59. Wilson WW, Walton JP (2002) Background noise improves gap detection in tonically inhibited inferior colliculus neurons. J Neurophysiol 87:240–249

    PubMed  Google Scholar 

  60. Winer JA, Schreiner CE (2005) The central auditory system: a functional analysis. In: Winer JA, Schreiner CE (eds) The Inferior Colliculus. Springer, New York

    Google Scholar 

  61. Yang L, Pollak GD (1997) Differential response properties of amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. J Neurophysiol 77:324–340

    CAS  PubMed  Google Scholar 

  62. Zhang H, Kelly JB (2003) Glutamatergic and GABAergic regulation of neural responses in inferior colliculus to amplitude-modulated sounds. J Neurophysiol 90:477–490

    CAS  Article  PubMed  Google Scholar 

  63. Zhang H, Kelly JB (2006) Responses of neurons in the rat’s ventral nucleus of the lateral lemniscus to amplitude-modulated tones. J Neurophysiol 96:2905–2914

    Article  PubMed  Google Scholar 

  64. Zheng Y, Escabi MA (2008) Distinct roles for onset and sustained activity in the neuronal code for temporal periodicity and acoustic envelope shape. J Neurosci 28:14230–14244

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  65. Zwicker E (1985) Temporal resolution in background noise. Br Audiol 19:9–12

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by NIH/National Institute on Deafness and Other Communication Disorders Grant RO1 DC-002266 to A.S.B. R.A.F. II was supported, in part, by training grant T32 GM081741 from the NIH/National Institute of General Medical Sciences to West Virginia University. A.K.M. was supported by the Swedish Research Council grants 80326601 and K2014-63X-22536-01-3.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Albert S. Berrebi.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Felix, R.A., Magnusson, A.K. & Berrebi, A.S. The superior paraolivary nucleus shapes temporal response properties of neurons in the inferior colliculus. Brain Struct Funct 220, 2639–2652 (2015). https://doi.org/10.1007/s00429-014-0815-8

Download citation

Keywords

  • Amplitude modulation
  • Gap detection
  • Superior olive
  • Sound envelopes
  • Temporal processing