Information Processing by Onset Neurons in the Cat Auditory Brainstem

Abstract

Octopus cells in the ventral cochlear nucleus (VCN) have been difficult to study because of the very features that distinguish them from other VCN neurons. We performed in vivo recordings in cats on well-isolated units, some of which were intracellularly labeled and histologically reconstructed. We found that responses to low-frequency tones with frequencies < 1 kHz reveal higher levels of neural synchrony and entrainment to the stimulus than the auditory nerve. In responses to higher frequency tones, the neural discharges occur mostly near the stimulus onset. These neurons also respond in a unique way to 100 % amplitude-modulated (AM) tones with discharges exhibiting a bandpass tuning. Responses to frequency-modulated sounds (FM) are unusual: Octopus cells react more vigorously during the ascending than the descending parts of the FM stimulus. We examined responses of neurons in the ventral nucleus of the lateral lemniscus (VNLL) whose discharges to tones and AM sounds are similar to octopus cells. Repeated stimulation with short tone pips of VCN and VNLL onset neurons evokes trains of action potentials with gradual shifts toward later times in their first spike latency. This behavior parallels short-term post-synaptic depression observed by other authors in in vitro VCN recordings of octopus cells. VCN and VNLL onset units in cats respond to frozen noise stimuli with gaps as narrow as 1 ms with a robust discharge near the stimulus onset following the gap. This finding suggests that VCN and VNLL onset cells play a role in gap detection, which is of great importance to speech perception.

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
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18
Fig. 19

References

  1. Abramson AS, Whalen DH (2017) Voice onset time (VOT) at 50: theoretical and practical issues in measuring voicing distinctions. J Phon 63:75–86

    PubMed  PubMed Central  Google Scholar 

  2. Adams JC (1997) Projections from octopus cells of the posteroventral cochlear nucleus to the ventral nucleus of the lateral lemniscus in cat and human. Auditory Neurosci 3:335–350

    Google Scholar 

  3. Aertesen AMHJ, Johannesma PIM (1980) Spectro-temporal receptive fields of auditory neurons in the grassfrog. Biol Cybernetics 38:223–234

    Google Scholar 

  4. Aitkin LM, Anderson DJ, Brugge JF (1970) Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. J Neurophysiol 33:421–440

    CAS  PubMed  Google Scholar 

  5. Batra R, Fitzpatrick DC (1999) Discharge patterns of neurons in the ventral nucleus of the lateral lemniscus of the unanesthetized rabbit. J Neurophysiol 82:1097–1113

    CAS  PubMed  Google Scholar 

  6. Bell A, Wit HP (2018) Cochlear impulse responses resolved into set of gammatones: the case for beating of closely spaced local resonances. PeerJ 6:e6016. https://doi.org/10.7717/peerj.6016

    Article  PubMed  PubMed Central  Google Scholar 

  7. Berger C, Meyer EMM, Ammer JJ, Felmy F (2014) Large somatic synapses on neurons in the ventral lateral lemniscus work in pairs. J Neurosci 34:3237–3246

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Borst JGG (2010) The low synaptic release probability in vivo. Trends Neurosci 33:259–266

    CAS  PubMed  Google Scholar 

  9. Britt R, Starr A (1976) Synaptic events and discharge patterns of cochlear nucleus cells. II Frequency-modulated tones. J Neurophysiol 39:179–194

    CAS  PubMed  Google Scholar 

  10. Davis KA, Lomakin O, Pesavento MJ (2007) Response properties of single units in the dorsal nucleus of the lateral lemniscus of decerebrate cats. J Neurophysiol 98:1475–1488

    PubMed  Google Scholar 

  11. Dicke U, Dau T (2005) A functional point-neuron model simulating cochlear nucleus ideal onset responses. J Comput Neurosci 19:239–253

    PubMed  Google Scholar 

  12. Fekete DM, Rouiller EM, Liberman MC, Ryugo DK (1984) The central projections of intracellularly labeled auditory nerve fibers in cats. J Comp Neurol 229:432–450

    CAS  PubMed  Google Scholar 

  13. Felix RA II, Gourévitch B, Gómez-Álvarez M, Leijon SCM, Saldaña E, Magnusson AK (2017) Octopus cells in the posteroventral cochlear nucleus provide the main excitatory input to the superior paraolivary nucleus. Front Neural Circuits 11:1–35. https://doi.org/10.3389/fncir.2017.00037

    CAS  Article  Google Scholar 

  14. Fujino K, Oertel D (2003) Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus. Proc Natl Acad Sci U S A 100:265–270

    CAS  PubMed  Google Scholar 

  15. Godfrey DA, Kiang NYS, Norris B (1975) Single unit activity in the posteroventral cochlear nucleus of the cat. J Comp Neurol 162:247–268

    CAS  PubMed  Google Scholar 

  16. 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 

  17. Golding NL, Oertel D (2012) Synaptic integration in dendrites: exceptional need for speed. J Physiol 590:5563–5569

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Golding NL, Robertson D, Oertel D (1995) Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. J Neurosci 15:3138–3153

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Gómez-Alvarez M, Gourévitch B, Felix RA II, Nyberg T, Hernández-Montiel HL, Magnusson AK (2018) Temporal information in tones, broadband noise and natural vocalizations is conveyed by differential spiking responses in the superior Paraolivary nucleus. Eur J Neurosci 48:2030–2049

    PubMed  Google Scholar 

  20. Harrison JM, Irving R (1966) The organization of the posterior ventral cochlear nucleus in the rat. J Comp Neurol 126:391–401

    CAS  PubMed  Google Scholar 

  21. Joris PX, Smith PH (2011) Octopus cells: the temporally most accurate in the brain? Assoc Res Otolaryngol Abs 677

  22. Joris PX, Carney LH, Smith PH, Yin TC (1994) Enhancement of neural synchronization in the anteroventral cochlear nucleus. I Responses to tones at the characteristic frequency J Neurophysiol 71:1022–1036

    CAS  PubMed  Google Scholar 

  23. Kadia SC, Wang X (2003) Spectral integration in A1 of awake primates: neurons with single- and multipeaked tuning characteristics. J Neurophysiol 89:1603–1622

    PubMed  Google Scholar 

  24. Kalluri S, Delgutte B (2003) Mathematical models of cochlear nucleus onset neurons: i. point neuron with many weak synaptic inputs. J Comput Neurosci 14:71–90

    PubMed  PubMed Central  Google Scholar 

  25. Keller CH, Takahashi TT (2000) Representation of temporal features of complex sounds by the discharge patterns of neurons in the owl’s inferior colliculus. J Neurophysiol 84:2638–2650

    CAS  PubMed  Google Scholar 

  26. Kim DG, Leonard G (1988) Responses of cochlear nucleus neurones to speech sounds. In: Moore BCJ, Patterson RD (eds) Auditory frequency selectivity, pp 281-288

  27. Kim PJ, Young ED (1994) Comparative analysis of spectro-temporal receptive fields, reverse correlation functions, and frequency tuning curves of auditory-nerve fibers. J Acoust Soc Am 95:410–422

    CAS  PubMed  Google Scholar 

  28. Klatt DH (1980) Software for a cascade/parallel formant synthesizer. J Acoust Soc Am 67:971–995

    Google Scholar 

  29. Kuenzel T (2019) Modulatory influences on time-coding neurons in the ventral cochlear nucleus. Hear Res 384:107824. https://doi.org/10.1016/j.heares.2019.107824

    Article  PubMed  Google Scholar 

  30. Kuenzel T, Borst JGG, van der Heijden M (2011) Factors controlling the input-output relationship of spherical bushy cells in the gerbil cochlear nucleus. J Neurosci 31:4260–4273

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Louage DHG, van der Heijden M, Joris PX (2005) Enhanced temporal response properties of anteroventral cochlear nucleus neurons to broadband noise. J Neurosci 25:1560–1570

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Lu H-W, Smith PH, Joris PX (2018) Submillisecond monaural coincidence detection by octopus cells. Acta Acust United Acust 104:852–855

    Google Scholar 

  33. Mardia KV (1972) Statistics of directional data. Academic Press, London

    Google Scholar 

  34. McGinley MC, Liberman MC, Bal R, Oertel D (2012) Generating synchrony from the asynchronous: compensation for cochlear traveling wave delays of individual brainstem neurons. J Neurosci 32:9301–9311

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Moore BCJ (2012) An introduction to the psychology of hearing. Sixth Edition, Brill

    Google Scholar 

  36. Oertel D (1997) Encoding of timing in the brain stem auditory nuclei of vertebrates. Neuron 19:959–962

    CAS  PubMed  Google Scholar 

  37. Oertel D, Wickesberg RE (2002) Ascending pathways through ventral nuclei of the lateral lemniscus and their possible role in pattern recognition in natural sounds. In: Oertel D, Fay RR (eds) Integrative functions in the mammalian auditory pathway, Springer, pp 207–237

  38. Oertel D, Bal R, Gardner SM, Smith PH, Joris PX (2000) Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. Proc Natl Acad Sci U S A 97:11773–11779

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Oertel D, Cao X-J, Ison JR, Allen PD (2017) Cellular computations underlying detection of gaps in sounds and lateralizing sound sources. Trends Neurosci 40:613–624

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Oertel D, Cao X-J, Recio-Spinoso A (2018) The cochlear nuclei: synaptic plasticity in circuits and synapses in the ventral cochlear nuclei. In: Kandler K (ed) The Oxford handbook of the auditory brainstem, Oxford University Press. https://doi.org/10.1093/oxfordhb/9780190849061.013.4

  41. Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–483

    CAS  PubMed  Google Scholar 

  42. Palmer AR, Winter IM (1993) Coding of fundamental frequency of voiced speech sounds and harmonic complex tones in the ventral cochlear nucleus. In: Merchan MA, Juiz DA, Godfrey DA, Mugnaini (eds) Mammalian cochlear nuclei. Plenum, pp 373–384

  43. Recio-Spinoso A (2012) Enhancement and distortion in the temporal representation of sounds in the ventral cochlear nucleus of chinchillas and cats. PLoS One 7:e44286. https://doi.org/10.1371/journal.pone.0044286

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Recio-Spinoso A, Joris PX (2014) Temporal properties of responses to sound in the ventral nucleus of the lateral lemniscus. J Neurophysiol 111:817–835

    PubMed  Google Scholar 

  45. Recio-Spinoso A, Narayan SS, Ruggero MA (2009) Basilar membrane responses to noise at a basal site of the chinchilla cochlea: quasi-linear filtering. J Assoc Res Otolaryngol 10:471–484

    PubMed  PubMed Central  Google Scholar 

  46. Rhode WS (1994) Temporal coding of 200% amplitude modulated signals in the ventral cochlear nucleus of cat. Hear Res 77:43–68

    CAS  PubMed  Google Scholar 

  47. Rhode WS (1998) Neural encoding of single-formant stimuli in the ventral cochlear nucleus of the chinchilla. Hear Res 117:39–56

    CAS  PubMed  Google Scholar 

  48. Rhode WS, Greenberg S (1994) Encoding of amplitude modulation in the cochlear nucleus of the cat. J Neurophysiol 71:1797–1825

    CAS  PubMed  Google Scholar 

  49. Rhode WS, Kettner RE (1987) Physiological study of neurons in the dorsal and posteroventral cochlear nucleus of the unanesthetized cat. J Neurophysiol 57:414–442

    CAS  PubMed  Google Scholar 

  50. Rhode WS, Smith PH (1986) Encoding timing and intensity in the ventral cochlear nucleus of the cat. J Neurophysiol 56:261–286

    CAS  PubMed  Google Scholar 

  51. Rhode WS, Oertel D, Smith PH (1983) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. J Comp Neurol 213:448–463

    CAS  PubMed  Google Scholar 

  52. Rice SO (1945) Mathematical analysis of random noise. Bell Syst Tech J 27:46–156

    Google Scholar 

  53. Rouiller EM, Ryugo DK (1984) Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J Comp Neurol 225:167–186

    CAS  PubMed  Google Scholar 

  54. Sakitt B (1973) Indices of discriminability. Nature 241:133–134

    CAS  PubMed  Google Scholar 

  55. Shannon RV, Zeng F-G, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303–304

    CAS  PubMed  Google Scholar 

  56. Smith PH, Massie A, Joris PX (2005) Acoustic stria: anatomy of physiologically characterized cells and their axonal projection patterns. J Comp Neurol 482:349–371

    PubMed  Google Scholar 

  57. Trussell LO (2018) In vitro studies of neuromodulation and plasticity in the dorsal cochlear nucleus. In: Kandler K (ed) The Oxford handbook of the auditory brainstem, Oxford University Press. https://doi.org/10.1093/oxfordhb/9780190849061.013.5

  58. Vater M, Covey E, Casseday JH (1997) The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus): synaptic arrangements and structural correlates of feedforward inhibitory function. Cell Tissue Res 289:223–233

    CAS  PubMed  Google Scholar 

  59. Viemeister NF, Plack CJ (1993) Time analysis. In: Yost WA, Popper AN, Fay RR (eds.) Human Psychophysics, Springer-Verlag pp. 116–154

  60. Viemeister NF, Shivapuja BG, Recio A (1992) Physiological correlates of temporal integration. In: Cazals Y, Horner K, Demany L (eds.) Auditory Physiology and Perception, Pergamon pp. 323–330

  61. Werner LA, Folsom RC, Mancl RL, Syapin CL (2001) Human auditory brainstem responses to temporal gaps in noise. J Speech Lang Hear Res 44:737–750

    CAS  PubMed  Google Scholar 

  62. Winter IM, Palmer AR (1995) Level dependence of cochlear nucleus onset unit responses and facilitation by second tones or broadband noise. J Neurophysiol 73:141–159

    CAS  PubMed  Google Scholar 

  63. Wu SH (1999) Physiological properties of neurons in the ventral nucleus of the lateral lemniscus of the rat: intrinsic membrane properties and synaptic responses. J Neurophysiol 81:2862–2874

    CAS  PubMed  Google Scholar 

  64. Yang H, Xu-Friedman MA (2015) Skipped-stimulus approach reveals that short-term plasticity dominates synaptic strength during ongoing activity. J Neurosci 35:8297–8307

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Young ED, Sachs MB (1979) Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers. J Acoust Soc Am 66:1381–1403

    CAS  PubMed  Google Scholar 

  66. Zeng F-G, Kong Y-Y, Michalewski HJ, Starr A (2005) Perceptual consequences of disrupted auditory nerve activity. J Neurophysiol 93:3050–3063

    PubMed  Google Scholar 

  67. Zhao M, Wu SH (2001) Morphology and physiology of neurons in the ventral nucleus of the lateral lemniscus in rat brain slices. J Comp Neurol 433:255–271

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thanks to histologists J. Ekleberry, J. Meister, and I. Sigglekow, to R. Kochhar for programming support, to K. Yentner for neuron reconstruction, to Philip Joris for all his help at KUL, and to Donata Oertel and David Ryugo for critiquing the manuscript. We also thank the two anonymous reviewers for their suggestions and comments.

Funding

The project was funded by the NIH-NIDCD DC17590, the Human Frontier Science Program, the Fund for Scientific Research-Flanders (G.0714.09), the Research Fund University of Leuven (OT/09/50), and the European Regional Development Fund.

Author information

Affiliations

Authors

Contributions

A.R.S. and W.S.R performed all aspects of this research, including designing the experiments, performing the experiments, analyzing the data, and writing the manuscript.

Corresponding author

Correspondence to Alberto Recio-Spinoso.

Ethics declarations

Experiments were performed at the University of Wisconsin, Madison, USA, and Katholieke Universiteit Leuven, Leuven, Belgium. At both locations, the work conformed to the animal use standards of the National Institutes of Health, USA, and was approved by the local animal care committee.

Competing Interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Recio-Spinoso, A., Rhode, W.S. Information Processing by Onset Neurons in the Cat Auditory Brainstem. JARO (2020). https://doi.org/10.1007/s10162-020-00757-0

Download citation

Keywords

  • cochlear nucleus
  • ventral nucleus of the lateral lemniscus
  • temporal processing
  • synaptic plasticity
  • gap detection