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Searching for an Internal Representation of Stimulus Kinematics in the Response of Ventral Paraflocculus Purkinje Cells

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Abstract

Motor control theories propose that the central nervous system builds internal representations of the motion of both our body and external objects. These representations, called forward models, are essential for accurate motor control. For instance, to produce a precise reaching movement to catch a flying ball, the central nervous system must build predictions of the current and future states of both the arm and the ball. Accumulating evidence suggests that the cerebellar cortex contains a forward model of an individual’s body movement. However, little evidence is yet available to suggest that it also contains a forward model of the movement of external objects. We investigated whether Purkinje cell simple spike responses in an oculomotor region of the cerebellar cortex called the ventral paraflocculus contained information related to the kinematics of behaviorally relevant visual stimuli. We used a visuomotor task that obliges animals to track moving targets while keeping their eyes fixated on a stationary target to separate signals related to visual tracking from signals related to eye movement. We found that ventral paraflocculus Purkinje cells do not contain information related to the kinematics of behaviorally relevant visual stimuli; they only contain information related to eye movements. Our data stand in contrast with data obtained from cerebellar Crus I, wherein Purkinje cell discharge contains information related to moving visual stimuli. Together, these findings suggest specialization in the cerebellar cortex, with some areas participating in the computation of our movement kinematics and others computing the kinematics of behaviorally relevant stimuli.

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References

  1. Wolpert DM, Miall RC. Forward models for physiological motor control. Neural Netw. 1996; 9(8): 1265–1279.

  2. Lacquaniti F, Maioli C. Adaptation to suppression of visual information during catching. Journal of Neuroscience. 1989;9:149–59.

    CAS  PubMed  Google Scholar 

  3. Ebner TJ, Pasalar S. Cerebellum predicts the future motor state. Cerebellum. 2008;7(4):583–8.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Herzfeld DJ, Kojima Y, Soetedjo R, Shadmehr R. Encoding of action by the Purkinje cells of the cerebellum. Nature. 2015;526(7573):439–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Wolpert DM, Kawato M. Multiple paired forward and inverse models for motor control. Neural Netw. 1998;11(7–8):1317–29.

    Article  CAS  PubMed  Google Scholar 

  6. Hewitt AL, Popa LS, Pasalar S, Hendrix CM, Ebner TJ. Representation of limb kinematics in Purkinje cell simple spike discharge is conserved across multiple tasks. J Neurophysiol. 2011;106(5):2232–47.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Frens MA, Donchin O. Forward models and state estimation in compensatory eye movements. Front Cell Neurosci. 2009 Nov 23;3:13.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Glasauer S. Cerebellar contribution to saccades and gaze holding: a modeling approach. Ann N Y Acad Sci. 2003 Oct;1004:206–19.

    Article  PubMed  Google Scholar 

  9. Popa LS, Hewitt AL, Ebner TJ. Purkinje cell simple spike discharge encodes error signals consistent with a forward internal model. Cerebellum 2013 Jun; 12(3):331–3. doi:10.1007/s12311-013-0452-4.

  10. Lisberger SG. Internal models of eye movement in the floccular complex of the monkey cerebellum. Neuroscience. 2009;162(3):763–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Miles OB, Cerminara NL, Marple-Horvat DE. Purkinje cells in the lateral cerebellum of the cat encode visual events and target motion during visually guided reaching. J Physiol. 2006 Mar 15;571(Pt 3):619–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cerminara NL, Apps R, Marple-Horvat DE. An internal model of a moving visual target in the lateral cerebellum. J Physiol. 2009 Jan 15;587(2):429–42.

    Article  CAS  PubMed  Google Scholar 

  13. Kuang S, Morel P, Gail A. Planning movements in visual and physical space in monkey posterior parietal cortex. Cereb Cortex. 2016;26(2):731–47.

    PubMed  Google Scholar 

  14. Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89(1):634–9.

    Article  PubMed  Google Scholar 

  15. O'Reilly JX, Mesulam MM, Nobre AC. The cerebellum predicts the timing of perceptual events. J Neurosci. 2008; 28(9): 2252–60.

  16. Blazquez PM, Hirata Y, Highstein SM. The vestibulo-ocular reflex as a model system for motor learning: what is the role of the cerebellum? Cerebellum. 2004;3(3):188–92.

    Article  PubMed  Google Scholar 

  17. Lisberger SG. Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning. J Neurophysiol. 1994;72(2):974–98.

    CAS  PubMed  Google Scholar 

  18. Escudero M, Cheron G, Godaux E. Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. II. Prepositus hypoglossal nucleus. J Neurophysiol. 1996;76(3):1775–85.

    CAS  PubMed  Google Scholar 

  19. Nakamagoe K, Iwamoto Y, Yoshida K. Evidence for brainstem structures participating in oculomotor integration. Science. 2000;288(5467):857–9.

    Article  CAS  PubMed  Google Scholar 

  20. Ghasia FF, Meng H, Angelaki DE. Neural correlates of forward and inverse models for eye movements: evidence from three-dimensional kinematics. J Neurosci. 2008;28(19):5082–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Langer T, Fuchs AF, Scudder CA, Chubb MC. Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol. 1985;235(1):1–25.

    Article  CAS  PubMed  Google Scholar 

  22. Graf W, Simpson JI, Leonard CS. Spatial organization of visual messages of the rabbit's cerebellar flocculus: II. Complex and simple spike responses of Purkinje cells. J Neurophysiol. 1988;60:2091–121.

    CAS  PubMed  Google Scholar 

  23. Stone LS, Lisberger SG. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys: II. Complex spikes. J Neurophysiol. 1990; 63:1 262–1275.

  24. Simpson JI, Alley KE. Visual climbing fiber input to rabbit vestibulo-cerebellum: a source of direction-specific information. Brain Res. 1974;82:302–8.

    Article  CAS  PubMed  Google Scholar 

  25. Laurens J, Heiney SA, Kim G, Blazquez PM. Cerebellar cortex granular layer interneurons in the macaque monkey are functionally driven by mossy fiber pathways through net excitation or inhibition. PLoS One. 2013 Dec;20:8(12).

    Google Scholar 

  26. Blazquez PM, Yakusheva TA. GABA-A inhibition shapes the spatial and temporal response properties of Purkinje cells in the macaque cerebellum. Cell Rep. 2015 May 19;11(7):1043–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lisberger SG, Westbrook LE. Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys. J Neurosci. 1985;5(6):1662–73.

    CAS  PubMed  Google Scholar 

  28. Akao T, Kumakura Y, Kurkin S, Fukushima J, Fukushima K. Directional asymmetry in vertical smooth-pursuit and cancellation of the vertical vestibulo-ocular reflex in juvenile monkeys. Exp Brain Res. 2007;182(4):469–78.

    Article  PubMed  Google Scholar 

  29. Hirata Y, Highstein SM. Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells. J Neurophysiol. 2001;85(5):2267–88.

    CAS  PubMed  Google Scholar 

  30. Suh M, Leung HC, Kettner RE. Cerebellar flocculus and ventral paraflocculus Purkinje cell activity during predictive and visually driven pursuit in monkey. J Neurophysiol. 2000;84(4):1835–50.

    CAS  PubMed  Google Scholar 

  31. Kettner RE, Suh M, Davis D, Leung HC. Complex predictive eye pursuit in monkey: a model system for cerebellar studies of skilled movement. Arch Ital Biol. 2002;140(4):331–40.

    CAS  PubMed  Google Scholar 

  32. Ono S, Das VE, Economides JR, Mustari MJ. Modeling of smooth pursuit-related neuronal responses in the DLPN and NRTP of the rhesus macaque. J Neurophysiol. 2005;93(1):108–16.

    Article  PubMed  Google Scholar 

  33. Stein JF, Glickstein M. Role of the cerebellum in visual guidance of movement. Physiol Rev. 1992;82:967–1017.

    Google Scholar 

  34. Coppe S, Orban de Xivry JJ, Yüksel D, Ivanoiu A, Lefèvre P. Dramatic impairment of prediction due to frontal lobe degeneration. J Neurophysiol. 2012;108(11):2957–66.

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Fanetta Hampton for animal care and training. We also thank her for helping with data collection and analysis. We are thankful for the financial support received from departmental funds (PMB) and from grants R01-NS065099 (PMB) and R01-NIDCD (TAY).

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Authors and Affiliations

  1. Department of Otolaryngology, Washington University School of Medicine, St. Louis, MO, 63110, USA

    Pablo M. Blazquez, GyuTae Kim & Tatyana A. Yakusheva

  2. Institute for Information and Electronics Research, Inha University, Incheon, South Korea

    GyuTae Kim

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  1. Pablo M. Blazquez
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  2. GyuTae Kim
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  3. Tatyana A. Yakusheva
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Corresponding author

Correspondence to Pablo M. Blazquez.

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The study conformed to the National Institutes of Health Guide for the Care and Use of Laboratory Animals and was approved by the Institutional Animal Care and Use Committee.

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The authors declare that they have no conflicts of interest.

Electronic Supplementary Material

Supplementary Figure 1

Response of an example Purkinje cell during two consecutive trials of the “Track-with-gap” task. a The green and red rectangles indicate the time when the green and red lasers are ON, respectively. b Eye position is represented by a solid trace, and red laser position is represented by a dashed traced. Note that the green laser position is always at 0°. c Raw neuronal data. Complex spikes are indicated with an asterisk. d Instantaneous firing rate (simple spikes). (PDF 409 kb)

Supplementary Figure 2

Neuronal response to saccades eye movements of the example cell shown in Figs. 3 and 5 during the “Track-with-gap” task and spontaneous saccades. Peristimulus time histograms were constructed with bin sizes of 20 ms that were aligned with saccade onset. The response to spontaneous saccades was extracted by using all spontaneous saccades with a dominant upward direction (45 to −45° from pure upward direction) and amplitudes of between 5 and 20°. Notice that the neuronal response latency to the saccade is the same for both spontaneous saccades and for saccades that occurred during the “Track-with-gap” task. (PDF 170 kb)

Supplementary Movie 1

Example showing the behavior of monkey A during the execution of the “Track-with-gap” task along the horizontal plane. The left panel shows an XY plot representation of the horizontal and vertical eye position (black start) and the horizontal and vertical red and green laser positions (red and green dots, respectively). In the right panel, the top three rows show the state of the reward, the green laser, and the red laser (high for on, low for off). The bottom two rows show changes in the positions of the eye and the red laser (black and red traces, respectively). (MOV 3707 kb)

Supplementary Movie 2

Example showing the behavior of monkey A during the execution of the “Track-with-gap” task along the vertical plane. The left panel shows an XY plot representation of the horizontal and vertical eye position (black start) and the horizontal and vertical red and green laser positions (red and green dots, respectively). In the right panel, the top three rows show the state of the reward, the green laser, and the red laser (high for on, low for off). The bottom two rows show changes in the positions of the eye and the red laser (black and red traces, respectively). (MOV 4740 kb)

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Blazquez, P.M., Kim, G. & Yakusheva, T.A. Searching for an Internal Representation of Stimulus Kinematics in the Response of Ventral Paraflocculus Purkinje Cells. Cerebellum 16, 817–826 (2017). https://doi.org/10.1007/s12311-017-0861-x

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