Skip to main content
SpringerLink
Log in

Non-associative learning processes in vestibular nucleus

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

Simple non-associative learning processes, habituation and sensitization, are known to be systemically involved in different neurotransmissions, and these processes in the vestibular nucleus (VN) often show opposite responding patterns to repeated stimuli. However, their roles and mechanisms of the reciprocal responses at the cellular level are still elusive. Here, we conducted an electrophysiological experiment to investigate the neuronal responses to repeated stimuli in the VN, characterizing the neuronal responding patterns of habituation and sensitization. Based on our results, we also suggested an alternative hypothesis that these non-associative neuronal responses generated biased neural information based on simple linear addition. Sixty-seven neuronal responses to repeated stimuli were recorded from 23 guinea pigs, and the habituated and the sensitized responses were 37 (range of slopes − 3.66~− 0.02 spks/s/trial) and 30 (0.01~1.51 spks/s/trial), respectively. Unlike previous study, the general neuronal responding shapes were not exponential, but most (94%, 63/67) responding profiles were linear. Although no strong relation between the irregular and the high sensitivity in our population, the neuronal irregularity and sensitivity could be the core factors to cause the biased results to more habituated side. In conclusion, we found that a biased neural response (mean ± STD − 0.22 ± 0.89 spks/s/trial) was constructed by two non-associative neuronal responses based on a linear addition of the slopes.

Hypothesized and calculated neural mediation by non-associative learning processes.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77(5):419–450

    Article  CAS  Google Scholar 

  2. Poon CS, Young DL (2006) Nonassociative learning as gated neural integrator and differentiator in stimulus-response pathways. Behav Brain Funct 2(29):29. https://doi.org/10.1186/1744-9081-2-29

    Article  PubMed  PubMed Central  Google Scholar 

  3. Clément G, Tilikete C, Courjon JH (2013) Influence of stimulus interval on the habituation of vestibulo-ocular reflex and sensation of rotation in humans. Neurosci Lett 549:40–44. https://doi.org/10.1016/j.neulet.2013.06.038

    Article  CAS  PubMed  Google Scholar 

  4. Courjon JH, Precht W, Sirkin DW (1987) Vestibular nerve and nuclei unit responses and eye movement responses to repetitive galvanic stimulation of the labyrinth in the rat. Exp Brain Res 66(1):41–48

    Article  CAS  Google Scholar 

  5. Kim J (2009) Short-term habituation of eye-movement responses induced by galvanic vestibular stimulation (GVS) in the alert Guinea pig. Brain Res Bull 79(1):1–5. https://doi.org/10.1016/j.brainresbull.2008.12.016

    Article  PubMed  Google Scholar 

  6. McSweeney FK, Murphy ES (2009) Sensitization and habituation regulate reinforcer effectiveness. Neurobiol Learn Mem 92(2):189–198. https://doi.org/10.1016/j.nlm.2008.07.002

    Article  PubMed  Google Scholar 

  7. Baird RA, Desmadryl G, Fernandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J Neurophysiol 60(1):182–203

    Article  CAS  Google Scholar 

  8. Balter SGT, Stokroos RJ, Akkermans E, Kingma H (2004a) Habituation to galvanic vestibular stimulation for analysis of postural control abilities in gymnasts. Neurosci Lett 366(1):71–75

    Article  CAS  Google Scholar 

  9. Kim HJ, Choi JY, Son EJ, Lee WS (2006) Response to galvanic vestibular stimulation in patients with unilateral vestibular loss. Laryngoscope 116(1):62–66

    Article  Google Scholar 

  10. Lee Son GM, Blouin J, Inglis JT (2008) Short-duration galvanic vestibular stimulation evokes prolonged balance responses. J Appl Physiol 105(4):1210–1217

    Article  Google Scholar 

  11. Wilkinson D, Zubko O, Sakel M, Coulton S, Higgins T, Pullicino P (2014) Galvanic vestibular stimulation in hemi-spatial neglect. Front Integr Neurosci 8(4). https://doi.org/10.3389/fnint.2014.00004

  12. Ezure K, Cohen M, Wilson V (1983) Response of cat semicircular canal afferents to sinusoidal polarizing currents: implications for input-output properties of second-order neurons. J Neurophysiol 49(3):639–648

    Article  CAS  Google Scholar 

  13. Goldberg JM, Smith CE, Fernandez C (1984) Relation between regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol 51(6):1236–1256

    Article  CAS  Google Scholar 

  14. Dieterich M, Zink R, Weiss A, Brandt T (1999) Galvanic stimulation in bilateral vestibular failure: 3-D ocular motor effects. Neuroreport 10(16):3283–3287

    Article  CAS  Google Scholar 

  15. Fitzpatrick R, Day B (2004) Probing the human vestibular system with galvanic stimulation. J Appl Physiol 96(6):2301–2316

    Article  Google Scholar 

  16. MacDougall HG, Brizuela AE, Curthoys IS (2003) Linearity, symmetry and additivity of the human eye-movement response to maintained unilateral and bilateral surface galvanic (DC) vestibular stimulation. Exp Brain Res 148(2):166–175

    Article  Google Scholar 

  17. Shanidze N, Lim K, Dye J, King WM (2012) Galvanic stimulation of the vestibular periphery in Guinea pigs during passive whole body rotation and self-generated head movement. J Neurophysiol 107(8):2260–2270

    Article  CAS  Google Scholar 

  18. Balter SGT, Stokroos RJ, Eterman RMA, Paredis SAB, Orbons J, Kingma H (2004b) Habituation to galvanic vestibular stimulation. Acta Otolaryngol 124(8):941–945

    Article  Google Scholar 

  19. Inglis JT, Shupert CL, Hlavacka F, Horak EB (1995) Effect of galvanic vestibular stimulation on human postural responses during support surface translations. J Neurophysiol 73(2):896–901

    Article  CAS  Google Scholar 

  20. Wardman DL, Day BL, Fitzpatrick RC (2003) Position and velocity responses to galvanic vestibular stimulation in human subjects during standing. J Physiol 547(Pt 1):293–299

    Article  CAS  Google Scholar 

  21. Angelaki DE, Perachio AA (1993) Contribution of irregular semicircular canal afferents to the horizontal vestibuloocular response constant velocity rotation. J Neurophysiol 69(3):996–999

    Article  CAS  Google Scholar 

  22. Minor L, Goldberg J (1991) Vestibular-nerve inputs to the vestibulo-ocular reflex: a functional-ablation study in the squirrel monkey. J Neurosci 11(6):1636–1648

    Article  CAS  Google Scholar 

  23. Cohen B, Yakushin S, Holstein G (2012) What does galvanic vestibular stimulation actually activate? Front Neurol 2(90). https://doi.org/10.3389/fneur.2011.00090

  24. Curthoys IS, MacDougall H (2012) What galvanic vestibular stimulation actually activates. Front Neurol 3(117). https://doi.org/10.3389/fneur.2011.00117

  25. Cauquil AS, Martinez P, Ouaknine M, Tardy-Gervet M (2000) Orientation of the body response to galvanic stimulation as a function of the inter-vestibular imbalance. Exp Brain Res 133(4):501–505

    Article  Google Scholar 

  26. Kim J (2013) Head movements suggest canal and otolith projections are activated during galvanic vestibular stimulation. Neuroscience 253:416–425. https://doi.org/10.1016/j.neuroscience.2013.08.058

    Article  CAS  PubMed  Google Scholar 

  27. Rizzo-Sierra CV, Gonzalez-Castaño A Leon-Sarmiento FE (2014)(2014) Galvanic vestibular stimulation: a novel modulatory countermeasure for vestibular-associated movement disorders. Arq Neuropsiquiatr 72(1):72–77

    Article  Google Scholar 

  28. Rapisarda C, Bacchelli B (1977) The brain of the Guinea pig in stereotaxic coordinates. Arch Sci Biol (Bologna) 61(1–4):1–37

    CAS  Google Scholar 

  29. Kim J, Curthoys IS (2004) Responses of primary vestibular neurons to galvanic vestibular stimulation (GVS) in the anaesthetized Guinea pig. Brain Res Bull 64(3):265–271

    Article  Google Scholar 

  30. Davie JT, Clark BA, Häusser M (2008) The origin of the complex spike in cerebellar Purkinje cells. J Neurosci 28(30):7599–7609

    Article  CAS  Google Scholar 

  31. Palmer LM, Clark BA, Gründemann J, Roth A, Stuart GJ, Häusser M (2010) Initiation of simple and complex spikes in cerebellar Purkinje cells. J Physiol 588(Pt 10):1709–1717

    Article  CAS  Google Scholar 

  32. Massot C, Chacron MJ, Cullen KE (2011) Information transmission and detection thresholds in the vestibular nuclei: single neurons vs. population encoding. J Neurophysiol 105(4):1798–1814

    Article  Google Scholar 

  33. Zink R, Bucher SF, Weiss A, Brandt TH, Dieterich M (1998) Effects of galvanic vestibular stimulation on otolithic and semicircular canal eye movements and perceived vertical. Electroencephalogr Clin Neurophysiol 107(3):200–205

    Article  CAS  Google Scholar 

  34. Eisenstein EM, Eisenstein D, Smith JC (2001) The evolutionary significance of habituation and sensitization across phylogeny: a behavioral homeostasis model. Integr Physiol Behav Sci 36(4):251–265

    Article  Google Scholar 

  35. Eisenstein EM, Eisenstein D (2006) A behavioral homeostasis theory of habituation and sensitization: II. Further developments and predictions. Rev Neurosci 17(5):533–557

    Article  CAS  Google Scholar 

  36. Dilda V, Morris TR, Yungher DA, MacDougall HG, Moore ST (2014) Central adaptation to repeated galvanic vestibular stimulation: implications for pre-flight astronaut training. Plos One 9(11):e112131. https://doi.org/10.1371/journal.pone.0112131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Melvill JG, Milsum JH (1971) Frequency-response analysis of central vestibular unit activity resulting from rotational stimulation of the semicircular canals. J Physiol 219(1):191–215

    Article  Google Scholar 

  38. Horn G, Hind RA (1970) Short-term changes in neural activity and behavior. Cambridge University Press, London

    Google Scholar 

  39. Castellucci V, Pinsker H, Kupfermann I, Kandel ER (1970) Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167(3926):1745–1748

    Article  CAS  Google Scholar 

  40. Kupfermann I, Castellucci V, Pinsker H, Kandel E (1970) Neuronal correlates of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167(3926):1743–1745

    Article  CAS  Google Scholar 

  41. Pinsker H, Kupfermann I, Castellucci V, Kandel E (1970) Habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167(3926):1740–1742

    Article  CAS  Google Scholar 

  42. Carew TJ, Castellucci VF, Kandel ER (1971) An analysis of dishabituation and sensitization of the gill-withdrawal reflex in Aplysia. Int J Neurosci 2(2):79–98

    Article  CAS  Google Scholar 

  43. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983a) Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J Neurophysiol 50(6):1522–1542

    Article  CAS  Google Scholar 

  44. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983b) Mechanoafferent neurons innervating tail of Aplysia. II. Modulation by sensitizing stimulation. J. Neurophysiol 50(6):1543–1559

    Article  CAS  Google Scholar 

  45. Bailey CH, Chen M (1988) Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc Natl Acad Sci U S A 85(7):2373–2377

    Article  CAS  Google Scholar 

  46. Cleary LJ, Lee WL, Byrne JH (1998) Cellular correlates of long-term sensitization in Aplysia. J Neuroscience 18(15):5988–5998

    Article  CAS  Google Scholar 

  47. Scholz KP, Byrne JH (1987) Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235(4789):685–687

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We specially thank SunHee Lee for the illustration of the brain.

Funding

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded partially by the Ministry of Education (2010-0020163 & NRF-2016R1D1A1B03930657).

Author information

Authors and Affiliations

  1. Institute for Information and Electronics Research, Inha University, High-Tech center #109, 100 Inharo, Namgu, Incheon, 402-751, Republic of Korea

    Gyutae Kim, Kyu-Sung Kim & Sangmin Lee

  2. Department of Otolaryngology—Head & Neck Surgery, Inha University Hospital, 27 Inhang-ro, Jung-Gu, Incheon, 400-711, Republic of Korea

    Kyu-Sung Kim

  3. Department of Electronic Engineering, Inha University, High-Tech center #704, 100 Inharo, Namgu, Incheon, 402-751, Republic of Korea

    Sangmin Lee

Authors
  1. Gyutae Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kyu-Sung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sangmin Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gyutae Kim.

Ethics declarations

All procedures and principles of laboratory animal care were approved by the Animal Ethics Committee at Inha University.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, G., Kim, KS. & Lee, S. Non-associative learning processes in vestibular nucleus. Med Biol Eng Comput 56, 1841–1851 (2018). https://doi.org/10.1007/s11517-018-1817-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-018-1817-0

Keywords

Search

Navigation