Advertisement

Influences of Motor Systems on Electrosensory Processing

  • Krista Perks
  • Nathaniel B. SawtellEmail author
Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 70)

Abstract

The first central stage of electrosensory processing in fish has proven to be a particularly useful model system for examining the general issue of how motor systems and behavior influence sensory processing. This chapter reviews this literature, focusing on a substantial body of work elucidating the synaptic, cellular, and circuit mechanisms for predicting and canceling self-generated sensory inputs. Some additional functions of motor corollary discharge signals in weakly electric mormyrid fish are also discussed along with the implications of studies on electrosensory systems for other sensory modalities and brain structures, including the auditory system and the cerebellum.

Keywords

Cerebellum Corollary discharge Dorsal cochlear nucleus Electric fish Electrosensory internal model Negative image Proprioception Reafference Synaptic plasticity 

Notes

Acknowledgments

This work was supported by grants from the National Science Foundation, the National Institutes of Health, and the Irma T. Hirschl Trust to Nathaniel B. Sawtell.

Compliance with Ethics Requirements

Krista Perks declares that she has no conflict of interest.

Nathaniel B. Sawtell declares that he has no conflict of interest.

References

  1. Amey-Ozel M, von der Emde G, Engelmann J, Grant K (2015) More a finger than a nose: the trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose fish Gnathonemus petersii. J Comp Neurol 523(5):769–789PubMedCrossRefGoogle Scholar
  2. Bastian J (1995) Pyramidal cell plasticity in weakly electric fish: a mechanism for attenuating responses to reafferent electrosensory inputs. J Comp Physiol A 176:63–78PubMedCrossRefGoogle Scholar
  3. Bastian AJ (2006) Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16(6):645–649PubMedCrossRefGoogle Scholar
  4. Bastian J, Bratton B (1990) Descending control of electroreception. I Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe. J Neurosci 10:1226–1240PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bastian J, Chacron MJ, Maler L (2004) Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41(5):767–779PubMedCrossRefGoogle Scholar
  6. Baumann O, Borra RJ, Bower JM, Cullen KE, Habas C, Ivry RB, Leggio M, Mattingley JB, Molinari M, Moulton EA, Paulin MG, Pavlova MA, Schmahmann JD, Sokolov AA (2015) Consensus paper: the role of the cerebellum in perceptual processes. Cerebellum 14(2):197–220PubMedCrossRefGoogle Scholar
  7. Bell C, Bodznick D, Montgomery J, Bastian J (1997a) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol 50:17–31PubMedCrossRefGoogle Scholar
  8. Bell C, von der Emde G (1995) Electric organ corollary discharge pathways in mormyrid fish. II The medial juxtalabar nucleus. J Comp Physiol A 177:463–479CrossRefGoogle Scholar
  9. Bell CC (1982) Properties of a modifiable efference copy in electric fish. J Neurophysiol 47:1043–1056PubMedCrossRefGoogle Scholar
  10. Bell CC (1986) Duration of plastic change in a modifiable efference copy. Brain Res 369:29–36PubMedCrossRefGoogle Scholar
  11. Bell CC (1989) Sensory coding and corollary discharge effects in mormyrid electric fish. J Exp Biol 146:229–253PubMedGoogle Scholar
  12. Bell CC (1990) Mormyromast electroreceptor organs and their afferents in mormyrid electric fish: II. Intra-axonal recordings show initial stages of central processing. J Neurophysiol 63:303–318PubMedCrossRefGoogle Scholar
  13. Bell CC (2001) Memory-based expectations in electrosensory systems. Curr Opin Neurobiol 11:481–487PubMedCrossRefGoogle Scholar
  14. Bell CC (2002) Evolution of cerebellum-like structures. Brain Behav Evol 59:312–326PubMedCrossRefGoogle Scholar
  15. Bell CC, Caputi A, Grant K, Serrier J (1993) Storage of a sensory pattern by anti-Hebbian synaptic plasticity in an electric fish. Proc Nat Acad Sci 90:4650–4654PubMedCrossRefGoogle Scholar
  16. Bell CC, Finger TE, Russell CJ (1981) Central connections of the posterior lateral line lobe in mormyrid fish. Exp Brain Res 42:9–22PubMedCrossRefGoogle Scholar
  17. Bell CC, Grant K (1989) Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish. J Neurosci 9:1029–1044PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bell CC, Han V, Sawtell NB (2008) Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1–24PubMedCrossRefGoogle Scholar
  19. Bell CC, Han VZ, Sugawara S, Grant K (1997b) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387:278–281PubMedCrossRefGoogle Scholar
  20. Bell CC, Libouban S, Szabo T (1983) Pathways of the electric organ discharge command and its corollary discharges in mormyrid fish. J Comp Neurol 216:327–338PubMedCrossRefGoogle Scholar
  21. Bell CC, Maler L (2005) Central neuroanatomy of electrosensory systems in fish. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 68–111CrossRefGoogle Scholar
  22. Bell CC, Russell CJ (1978) Effect of electric organ discharge on ampullary receptors in a mormyrid. Brain Res 145:85–96PubMedCrossRefGoogle Scholar
  23. Berrebi AS, Morgan JI, Mugnaini E (1990) The Purkinje cell class may extend beyond the cerebellum. J Neurocytol 19(5):643–654PubMedCrossRefGoogle Scholar
  24. Bodznick D, Montgomery JC, Carey M (1999) Adaptive mechanisms in the elasmobranch hindbrain. J Exp Biol 202:1357–1364PubMedGoogle Scholar
  25. Borges-Merjane C, Trussell LO (2015) ON and OFF unipolar brush cells transform multisensory inputs to the auditory system. Neuron 85(5):1029–1042PubMedPubMedCentralCrossRefGoogle Scholar
  26. Brooks JX, Carriot J, Cullen KE (2015) Learning to expect the unexpected: rapid updating in primate cerebellum during voluntary self-motion. Nat Neurosci 18(9):1310–1317PubMedPubMedCentralCrossRefGoogle Scholar
  27. Brooks JX, Cullen KE (2013) The primate cerebellum selectively encodes unexpected self-motion. Curr Biol 23(11):947–955PubMedPubMedCentralCrossRefGoogle Scholar
  28. Campbell HR, Meek J, Zhang J, Bell CC (2007) Anatomy of the posterior caudal lobe of the cerebellum and the eminentia granularis posterior in a mormyrid fish. J Comp Neurol 502(5):714–735PubMedCrossRefGoogle Scholar
  29. Cant NB (1992) The cochlear nucleus: neuronal types and their synaptic organization. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 66–116CrossRefGoogle Scholar
  30. Carlson BA (2002) Neuroanatomy of the mormyrid electromotor control system. J Comp Neurol 454:440–455PubMedCrossRefGoogle Scholar
  31. Churchland PS, Ramachandran VS, Sejnowski TJ (1994) A critique of pure vision. In: Koch C, Davis JL (eds) Large-scale neuronal theories of the brain. MIT Press, Cambridge, pp 23–74Google Scholar
  32. Crapse TB, Sommer MA (2008) Corollary discharge across the animal kingdom. Nat Rev Neurosci 9(8):587–600PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dean P, Porrill J, Stone JV (2002) Decorrelation control by the cerebellum achieves oculomotor plant compensation in simulated vestibulo-ocular reflex. Proc Biol Sci 269(1503):1895–1904PubMedPubMedCentralCrossRefGoogle Scholar
  34. Duman CH, Bodznick D (1996) A role for GABAergic inhibition in electrosensory processing and common mode rejection in the dorsal nucleus of the little skate, Raja erinacea. J Comp Physiol A 179:797–807PubMedCrossRefGoogle Scholar
  35. Ebner TJ, Pasalar S (2008) Cerebellum predicts the future motor state. Cerebellum 7(4):583–588PubMedPubMedCentralCrossRefGoogle Scholar
  36. Engelmann J, Nobel S, Rover T, Emde G (2009) The Schnauzenorgan-response of Gnathonemus petersii. Front Zool 6:21PubMedPubMedCentralCrossRefGoogle Scholar
  37. Enikolopov AG, Abbott LF, Sawtell NB (2018) Internally generated predictions enhance neural and behavioral detection of sensory stimuli in an electric fish. Neuron 99(1):135–146PubMedPubMedCentralCrossRefGoogle Scholar
  38. Finger TE, Bell CC, Carr C (1986) Comparisons among electroreceptive teleosts: why are the electrosensory systems so similar? In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 465–481Google Scholar
  39. Fotowat H, Harrison RR, Krahe R (2013) Statistics of the electrosensory input in the freely swimming weakly electric fish Apteronotus leptorhynchus. J Neurosci 33(34):13758–13772PubMedPubMedCentralCrossRefGoogle Scholar
  40. Fujita M (1982) Adaptive filter model of the cerebellum. Biol Cybern 45(3):195–206PubMedCrossRefGoogle Scholar
  41. Gibson JJ (1979) The ecological approach to visual perception. Houghton Mifflin, BostonGoogle Scholar
  42. Grant K, Sugawara S, Gomez L, Han VZ, Bell CC (1998) The Mormyrid electrosensory lobe in vitro: physiology and pharmacology of cells and circuits. J Neurosci 18:6009–6025PubMedPubMedCentralCrossRefGoogle Scholar
  43. Grusser OJ (1986) Interaction of efferent and afferent signals in visual perception: a history of ideas and experimental paradigms. Acta Psychol 63:3–21CrossRefGoogle Scholar
  44. Hall JC, Bell C, Zelick R (1995) Behavioral evidence of a latency code for stimulus intensity in mormyrid electric fish. J Comp Physiol A 177:29–39CrossRefGoogle Scholar
  45. Halverson HE, Khilkevich A, Mauk MD (2015) Relating cerebellar purkinje cell activity to the timing and amplitude of conditioned eyelid responses. J Neurosci 35:7813–7832PubMedPubMedCentralCrossRefGoogle Scholar
  46. Han VZ, Grant G, Bell CC (2000) Reversible associative depression and nonassociative potentiation at a parallel fiber synapse. Neuron 27:611–622PubMedCrossRefGoogle Scholar
  47. Harvey-Girard E, Lewis J, Maler L (2010) Burst-induced anti-Hebbian depression acts through short-term synaptic dynamics to cancel redundant sensory signals. J Neurosci 30:6152–6169PubMedPubMedCentralCrossRefGoogle Scholar
  48. Hofmann V, Sanguinetti-Scheck JI, Gomez-Sena L, Engelmann J (2017) Sensory flow as a basis for a novel distance cue in freely behaving electric fish. J Neurosci 37:302–312PubMedPubMedCentralCrossRefGoogle Scholar
  49. Ito M (1984) The cerebellum and neural control. Raven Press, New YorkGoogle Scholar
  50. Jirenhed DA, Hesslow G (2011) Learning stimulus intervals--adaptive timing of conditioned purkinje cell responses. Cerebellum 10(3):523–535PubMedCrossRefGoogle Scholar
  51. Johansson F, Jirenhed DA, Rasmussen A, Zucca R, Hesslow G (2014) Memory trace and timing mechanism localized to cerebellar Purkinje cells. Proc Natl Acad Sci U S A 111(41):14930–14934PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kennedy A, Wayne G, Kaifosh P, Alvina K, Abbott LF, Sawtell NB (2014) A temporal basis for predicting the sensory consequences of motor commands in an electric fish. Nat Neurosci 17:416–422PubMedPubMedCentralCrossRefGoogle Scholar
  53. Litwin-Kumar A, Harris KD, Axel R, Sompolinsky H, Abbott LF (2017) Optimal degrees of synaptic connectivity. Neuron 93:1153–1164PubMedPubMedCentralCrossRefGoogle Scholar
  54. Machado AS, Darmohray DM, Fayad J, Marques HG, Carey MR (2015) A quantitative framework for whole-body coordination reveals specific deficits in freely walking ataxic mice. elife 4:e07892PubMedPubMedCentralCrossRefGoogle Scholar
  55. Markram H, Gerstner W, Sjostrom PJ (2011) A history of spike-timing-dependent plasticity. Front Synaptic Neurosci 3:4PubMedPubMedCentralCrossRefGoogle Scholar
  56. Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD (2000a) Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20:5516–5525PubMedPubMedCentralCrossRefGoogle Scholar
  57. Medina JF, Mauk MD (2000) Computer simulation of cerebellar information processing. Nat Neurosci 3:1205–1211PubMedCrossRefGoogle Scholar
  58. Medina JF, Nores WL, Ohyama T, Mauk MD (2000b) Mechanisms of cerebellar learning suggested by eyelid conditioning. Curr Opin Neurobiol 10:717–724PubMedCrossRefGoogle Scholar
  59. Meek J, Grant K, Bell C (1999) Structural organization of the mormyrid electrosensory lateral line lobe. J Exp Biol 202:1291–1300PubMedGoogle Scholar
  60. Meek J, Grant K, Sugawara S, Hafmans TGM, Veron M, Denizot JP (1996) Interneurons of the ganglionic layer in the mormyrid electrosensory lateral line lobe: morphology, immunocytochemistry, and synaptology. J Comp Neurol 375:43–65PubMedCrossRefGoogle Scholar
  61. Montgomery JC (1984) Noise cancellation in the electrosensory system of the thornback ray; common mode rejection of input produced by the animal's own ventilatory movement. J Comp Physiol A 155:103–111CrossRefGoogle Scholar
  62. Montgomery JC, Bodznick D (1994) An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish. Neurosci Lett 174:145–148PubMedCrossRefGoogle Scholar
  63. Montgomery JC, Bodznick D (1999) Signals and noise in the elasmobranch electrosensory system. J Exp Biol 202:1349–1355PubMedGoogle Scholar
  64. Mugnaini E, Maler L (1987) Cytology and immunohistochemistry of the nucleus exterlateralis anterior of the mormyrid brain: possible role of GABAergic synapses in temporal analysis. Anat Embryol 176:313–336PubMedCrossRefGoogle Scholar
  65. Mugnaini E, Sekerkova G, Martina M (2011) The unipolar brush cell: a remarkable neuron finally receiving deserved attention. Brain Res Rev 66:220–245PubMedCrossRefGoogle Scholar
  66. Nelson ME, Paulin MG (1995) Neural simulations of adaptive reafference suppression in the elasmobranch electrosensory system. J Comp Physiol A 177:723–736PubMedCrossRefGoogle Scholar
  67. Nixon DP, Passingham RE (2001) Predicting sensory events: the role of the cerebellum in motor learning. Exp Brain Res 138:251–257PubMedCrossRefGoogle Scholar
  68. Oertel D, Young ED (2004) What's a cerebellar circuit doing in the auditory system? Trends Neurosci 27:104–110PubMedCrossRefGoogle Scholar
  69. Ohyama T, Nores WL, Murphy M, Mauk MD (2003) What the cerebellum computes. Trends Neurosci 26:222–227PubMedCrossRefGoogle Scholar
  70. Pasalar S, Roitman AV, Durfee WK, Ebner TJ (2006) Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci 9:1404–1411PubMedCrossRefGoogle Scholar
  71. Pereira AC, Centurion V, Caputi AA (2005) Contextual effects of small environments on the electric images of objects and their brain evoked responses in weakly electric fish. J Exp Biol 208:961–972PubMedCrossRefGoogle Scholar
  72. Post N, von der Emde G (1999) The ‘novelty response’ in an electric fish: response properties and habituation. Physiol Behav 68:115–128PubMedCrossRefGoogle Scholar
  73. Prechtl JC, von der Emde G, Wolfart J, Karamursel S, Akoev GN, Andrianov YN, Bullock TH (1998) Sensory processing in the pallium of a mormyrid fish. J Neurosci 18:7381–7393PubMedPubMedCentralCrossRefGoogle Scholar
  74. Requarth T, Sawtell NB (2014) Plastic corollary discharge predicts sensory consequences of movements in a cerebellum-like circuit. Neuron 82(4):896–907PubMedPubMedCentralCrossRefGoogle Scholar
  75. Roberts PD (1999) Computational consequences of temporally asymmetric learning rules: I. Differential hebbian learning. J Comp Neurosci 7:235–246CrossRefGoogle Scholar
  76. Roberts PD, Bell CC (2000) Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. J Comput Neurosci 9(1):67–83PubMedCrossRefGoogle Scholar
  77. Russell CJ, Bell CC (1978) Neuronal responses to electrosensory input in the mormyrid valvula cerebelli. J Neurophysiol 41:1495–1510PubMedCrossRefGoogle Scholar
  78. Sawtell NB (2010) Multimodal integration in granule cells as a basis for associative plasticity and sensory prediction in a cerebellum-like circuit. Neuron 66(4):573–584PubMedCrossRefGoogle Scholar
  79. Sawtell NB, Williams A (2008) Transformations of electrosensory encoding associated with an adaptive filter. J Neurosci 28(7):1598–1612PubMedPubMedCentralCrossRefGoogle Scholar
  80. Sawtell NB, Williams A, Bell CC (2007) Central control of dendritic spikes shapes the responses of Purkinje-like cells through spike timing-dependent synaptic plasticity. J Neurosci 27:1552–1565PubMedPubMedCentralCrossRefGoogle Scholar
  81. Singla S, Dempsey C, Warren R, Enikolopov AG, Sawtell NB (2017) A cerebellum-like circuit in the auditory system cancels responses to self-generated sounds. Nat Neurosci 20:943–950PubMedPubMedCentralCrossRefGoogle Scholar
  82. Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43:482–489PubMedCrossRefGoogle Scholar
  83. Sun LD, Goldberg ME (2016) Corollary discharge and oculomotor proprioception: cortical mechanisms for spatially accurate vision. Annu Rev Vis Sci 2:61–84PubMedPubMedCentralCrossRefGoogle Scholar
  84. Szabo T, Hagiwara S (1967) A latency-change mechanism involved in sensory coding of electric fish (mormyrids). Physiol Behav 2:331–335CrossRefGoogle Scholar
  85. Toerring MJ, Moller P (1984) Locomotor and electric displays associated with electrolocation during exploratory behavior in mormyrid fish. Behav Brain Res 12:291–306PubMedCrossRefGoogle Scholar
  86. Tzounopoulos T, Kim Y, Oertel D, Trussell LO (2004) Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7:719–725PubMedCrossRefGoogle Scholar
  87. Tzounopoulos T, Rubio ME, Keen JE, Trussell LO (2007) Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing-dependent plasticity. Neuron 54:291–301PubMedPubMedCentralCrossRefGoogle Scholar
  88. von der Emde G, Bell C (1996) Nucleus preeminentialis of mormyrid fish, a center for recurrent electrosensory feedback. I. Electrosensory and corollary discharge responses. J Neurophysiol 76:1581–1596PubMedCrossRefGoogle Scholar
  89. von der Emde G, Sena LG, Niso R, Grant K (2000) The midbrain precommand nucleus of the mormyrid electromotor network. J Neurosci 20:5483–5495PubMedPubMedCentralCrossRefGoogle Scholar
  90. von Holst E, Mittelstaedt H (1950) The reafference principle. Naturwissenschaften 37:464–476CrossRefGoogle Scholar
  91. Zhang J, Han VZ, Meek J, Bell CC (2007) Granular cells of the mormyrid electrosensory lobe and postsynaptic control over presynaptic spike occurrence and amplitude through an electrical synapse. J Neurophysiol 9(3):2191–2203CrossRefGoogle Scholar
  92. Zhang Z, Bodznick D (2008) Plasticity in a cerebellar-like structure: suppressing reafference during episodic behaviors. J Exp Biol 211:3720–3728PubMedCrossRefGoogle Scholar
  93. Zhang Z, Bodznick D (2010) The importance of N-methyl-D-aspartate (NMDA) receptors in subtraction of electrosensory reafference in the dorsal nucleus of skates. J Exp Biol 213:2700–2709PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Zuckerman Mind Brain Behavior Institute, Department of Neuroscience and Kavli Institute for Brain Science, Columbia University, Jerome L. Greene Science CenterNew YorkUSA

Personalised recommendations