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.
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References
Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77(5):419–450
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
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
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
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
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
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
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
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
Lee Son GM, Blouin J, Inglis JT (2008) Short-duration galvanic vestibular stimulation evokes prolonged balance responses. J Appl Physiol 105(4):1210–1217
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
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
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
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
Fitzpatrick R, Day B (2004) Probing the human vestibular system with galvanic stimulation. J Appl Physiol 96(6):2301–2316
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
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
Balter SGT, Stokroos RJ, Eterman RMA, Paredis SAB, Orbons J, Kingma H (2004b) Habituation to galvanic vestibular stimulation. Acta Otolaryngol 124(8):941–945
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
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
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
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
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
Curthoys IS, MacDougall H (2012) What galvanic vestibular stimulation actually activates. Front Neurol 3(117). https://doi.org/10.3389/fneur.2011.00117
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
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
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
Rapisarda C, Bacchelli B (1977) The brain of the Guinea pig in stereotaxic coordinates. Arch Sci Biol (Bologna) 61(1–4):1–37
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
Davie JT, Clark BA, Häusser M (2008) The origin of the complex spike in cerebellar Purkinje cells. J Neurosci 28(30):7599–7609
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
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
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
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
Eisenstein EM, Eisenstein D (2006) A behavioral homeostasis theory of habituation and sensitization: II. Further developments and predictions. Rev Neurosci 17(5):533–557
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
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
Horn G, Hind RA (1970) Short-term changes in neural activity and behavior. Cambridge University Press, London
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
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
Pinsker H, Kupfermann I, Castellucci V, Kandel E (1970) Habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167(3926):1740–1742
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
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
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
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
Cleary LJ, Lee WL, Byrne JH (1998) Cellular correlates of long-term sensitization in Aplysia. J Neuroscience 18(15):5988–5998
Scholz KP, Byrne JH (1987) Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235(4789):685–687
Acknowledgements
We specially thank SunHee Lee for the illustration of the brain.
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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).
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All procedures and principles of laboratory animal care were approved by the Animal Ethics Committee at Inha University.
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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
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DOI: https://doi.org/10.1007/s11517-018-1817-0