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From cerebellar texture to movement optimization

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Abstract

The cerebellum is a major site for supervised procedural learning and appears to be crucial for optimizing sensorimotor performance. However, the site and origin of the supervising signal are still elusive. Furthermore, its relationship with the prominent neuronal circuitry remains puzzling. In this paper, I will review the relevant information and seek to synthesize a working hypothesis that explains the unique cerebellar structure. The aim of this review was to link the distinctive functions of the cerebellum, as derived from cerebellar lesion studies, with potential elementary computations, as observed by a bottom-up approach from the cerebellar microcircuitry. The parallel fiber geometry is ideal for performing millisecond computations that extract instructive signals. In this scenario, the higher time derivatives of kinematics such as acceleration and/or jerk that occur during motor performance are detected via a tidal wave mechanism and are used (with appropriate gating) as the instructive signal to guide motor smoothing. The advantage of such a mechanism is that movements are optimized by reducing “jerkiness” which, in turn, lowers their energy requirements.

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Abbreviations

CF:

Climbing fiber

CS:

Complex spike

DCN:

Deep cerebellar nuclei

GrC:

Granule cells

IO:

Inferior olive

MF:

Mossy fibers

PC:

Purkinje cell

PF:

Parallel fibers

TW:

Tidal wave

References

  • Adams DL, Horton JC (2003) A precise retinotopic map of primate striate cortex generated from the representation of angioscotomas. J Neurosci 23(9):3771–3789

    CAS  PubMed  Google Scholar 

  • Albus J (1971) A theory of cerebellar function. Math Biosci 10:25–61

    Article  Google Scholar 

  • Andersson G, Hesslow G (1987) Cerebellar inhibition of the inferior olive. In: Glickstein M, Yeo C, Stein J (eds) Cerebellum and neuronal plasticity. Plenum Press, New York, pp 141–154

    Chapter  Google Scholar 

  • Barash S, Melikyan A, Sivakov A, Zhang M, Glickstein M, Thier P (1999) Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. J Neurosci 19(24):10931–10939

    CAS  PubMed  Google Scholar 

  • Ben-Itzhak S, Karniel A (2007) Minimum acceleration criterion with constraints implies bang-bang control as an underlying principle for optimal trajectories of arm reaching movements. Neural Comput 20(3):779–812. doi:10.1162/neco.2007.12-05-077

    Article  Google Scholar 

  • Bengtsson F, Hesslow G (2006) Cerebellar control of the inferior olive. Cerebellum 5(1):7–14. doi:10.1080/14734220500462757

    Article  CAS  PubMed  Google Scholar 

  • Bernstein NA (1967) The co-ordination and regulation of movements. 1st English edn. Pergamon Press, Oxford

    Google Scholar 

  • Bosco G, Poppele RE (2001) Proprioception from a spinocerebellar perspective. Physiol Rev 81(2):539–568

    CAS  PubMed  Google Scholar 

  • Bower JM, Beermann DH, Gibson JM, Shambes GM, Welker W (1981) Principles of organization of a cerebro-cerebellar circuit. Micromapping the projections from cerebral (SI) to cerebellar (granule cell layer) tactile areas of rats. Brain Behav Evol 18(1–2):1–18

  • Bower JM, Woolston DC (1983) Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J Neurophysiol 49:745–766

    CAS  PubMed  Google Scholar 

  • Braitenberg V (1961) Functional interpretation of cerebellar histology. Nature 190:539–540

    Article  Google Scholar 

  • Braitenberg V (1983) The cerebellum revisited. J Theor Neurobiol 2:237–241

    Google Scholar 

  • Braitenberg V (1987) The cerebellum and the physics of movement: some speculations. In: Glickstein M, Yeo C, Stein J (eds) Cerebellum and neuronal plasticity. Plenum Press, New York, pp 193–208

    Chapter  Google Scholar 

  • Braitenberg V, Atwood RP (1958) Morphological observations on the cerebellar cortex. J Comp Neurol 109:1–34

    Article  CAS  PubMed  Google Scholar 

  • Braitenberg V, Heck D, Sultan F (1997) The detection and generation of sequences as a key to cerebellar function: experiments and theory. Behav Brain Sci 20(2):229–245

    Article  CAS  PubMed  Google Scholar 

  • Brindley GS (1964) The use made by the cerebellum of the information that it receives from sense organs. Int Brain Res Org Bull 3:80

    Google Scholar 

  • Capelli C, Prendergast DR, Termin B (1998) Energetics of swimming at maximal speeds in humans. Eur J Appl Physiol Occup Physiol 78(5):385–393. doi:10.1007/s004210050435

  • Catz N, Dicke PW, Thier P (2008) Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response. Proc Natl Acad Sci USA 105(20):7309–7314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cerminara NL, Makarabhirom K, Rawson JA (2003) Somatosensory properties of cuneocerebellar neurones in the main cuneate nucleus of the rat. Cerebellum 2(2):131–145

    Article  PubMed  Google Scholar 

  • Colwin C (1992) Swimming into the 21st century. Leisure Press, Champaign

    Google Scholar 

  • Dean P, Porrill J, Ekerot C-F, Jörntell H (2009) The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat Rev Neurosci 11(1):30–43. doi:10.1038/nrn2756

    Article  PubMed  Google Scholar 

  • Diedrichsen J, Criscimagna-Hemminger SE, Shadmehr R (2007) Dissociating timing and coordination as functions of the cerebellum. J Neurosci 27(23):6291–6301. doi:10.1523/jneurosci.0061-07.2007

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eccles JC, Ito M, Szentagothai J (1967) The cerebellum as a neuronal machine. Springer, Berlin

    Book  Google Scholar 

  • Edgley SA, Gallimore CM (1988) The morphology and projections of dorsal horn spinocerebellar tract neurones in the cat. J Physiol 397:99–111

    CAS  PubMed Central  PubMed  Google Scholar 

  • Flash T, Hogan N (1985) The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 7:1688– 1703

  • Fujita M (1982) Adaptive filter model of the cerebellum. Biol Cybern 45:195–206

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, van Beugen BJ, De Zeeuw CI (2012) Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci 13(9):619– 635

  • Gellman R, Gibson AR, Houk JC (1985) Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. J Neurophysiol 54:40–60

    CAS  PubMed  Google Scholar 

  • Gibson AR, Horn KM, Pong M (2004) Activation of climbing fibers. Cerebellum 3(4):212–221. doi:10.1080/14734220410018995

  • Glickstein M, Strata P, Voogd J (2009) Cerebellum: history. Neuroscience 162(3):549–559. doi:10.1016/j.neuroscience.2009.02.054

    Article  CAS  PubMed  Google Scholar 

  • Glickstein M, Sultan F, Voogd J (2011) Functional localization in the cerebellum. Cortex 47(1):59–80. doi:10.1016/j.cortex.2009.09.001

    Article  PubMed  Google Scholar 

  • Grosche J, Kettenmann H, Reichenbach A (2002) Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neurosci Res 68(2):138–149

    Article  CAS  PubMed  Google Scholar 

  • Hall AC, Lucas FR, Salinas PC (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100(5):525–535

    Article  CAS  PubMed  Google Scholar 

  • Hamodeh S, Eicke D, Napper RMA, Harvey RJ, Sultan F (2010) Population based quantification of dendrites: evidence for the lack of microtubule-associate protein 2a, b in Purkinje cell spiny dendrites. Neuroscience 170(4):1004–1014. doi:10.1016/j.neuroscience.2010.08.021

    Article  CAS  PubMed  Google Scholar 

  • Hamori J, Somogyi J (1983) Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J Comp Neurol 220(4):365–377

    Article  CAS  PubMed  Google Scholar 

  • Harvey RJ, Napper RMA (1991) Quantitative studies on the mammalian cerebellum. Prog Neurobiol 36:437–463

    Article  CAS  PubMed  Google Scholar 

  • Heck D (1993) Rat cerebellar cortex in-vitro responds specifically to moving stimuli. Neurosci Lett 157:95–98

    Article  CAS  PubMed  Google Scholar 

  • Heck D (1995) Die Bedeutung raum-zeitlicher Dynamik für die Aktivität des Kleinhirnkortex und die Interpretation seiner Anatomie. Verlag Dr. Kovac, Hamburg

    Google Scholar 

  • Heck D, Sultan F, Braitenberg V (2001) Sequential stimulation of rat cerebellar granular layer in vivo: further evidence of a ‘tidal-wave’ timing mechanism in the cerebellum. Neurocomputing 38: 641–646

  • Heck DH, Thach WT, Keating JG (2007) On-beam synchrony in the cerebellum as the mechanism for the timing and coordination of movement. Proc Natl Acad Sci 104(18):7658–7663. doi:10.1073/pnas.0609966104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hillman DE (1969) Neuronal organization of the cerebellar cortex in amphibia and reptilia. In: Llinás RR (ed) Neurobiology of cerebellar evolution and development. American Medical Association, Chicago, pp 279–325

    Google Scholar 

  • Hogan N (1984) An organizing principle for a class of voluntary movements. J Neurosci 4:2745–2754

    CAS  PubMed  Google Scholar 

  • Hore J, Timmann D, Watts S (2002) Disorders in timing and force of finger opening in overarm throws made by cerebellar subjects. Ann NY Acad Sci 978:1–15

    Article  CAS  PubMed  Google Scholar 

  • Isope P, Barbour B (2002) Properties of unitary granule cell\(\rightarrow \)Purkinje cell synapses in adult rat cerebellar slices. J Neurosci 22(22):9668–9678

  • Ito M (2002a) Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann N Y Acad Sci 978:273–288

    Article  PubMed  Google Scholar 

  • Ito M (2002b) The molecular organization of cerebellar long-term depression. Nat Rev Neurosci 3(11):896–902

    Article  CAS  PubMed  Google Scholar 

  • Jacobson M (1962) The representation of the retina on the optic tectum of the frog. Correlation between retinotectal magnification factor and retinal ganglion cell count. Q J Exp Physiol Cogn Med Sci 47:170–178

    CAS  PubMed  Google Scholar 

  • Lefler Y, Yarom Y, Uusisaari MY (2014) Cerebellar inhibitory input to the inferior olive decreases electrical coupling and blocks subthreshold oscillations. Neuron 81(6):1389–1400. doi:10.1016/j.neuron.2014.02.032

    Article  CAS  PubMed  Google Scholar 

  • Luo L, Flanagan JG (2007) Development of continuous and discrete neural maps. Neuron 56(2):284–300. doi:10.1016/j.neuron.2007.10.014

    Article  CAS  PubMed  Google Scholar 

  • Marr D (1969) A theory of cerebellar cortex. J Physiol Lond 202:437–470

    CAS  PubMed Central  PubMed  Google Scholar 

  • Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD (2000) Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20(14):5516–5525

    CAS  PubMed  Google Scholar 

  • Medina JF, Mauk MD (2000) Computer simulation of cerebellar information processing. Nat Neurosci 3(Suppl):1205–1211

    Article  CAS  PubMed  Google Scholar 

  • Miles FA (1997) Visual stabilization of the eyes in primates. Curr Opin Neurobiol 7(6):867–871

    Article  CAS  PubMed  Google Scholar 

  • Miles FA, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibuloocular reflex. IV. Electrophysiological observations in flocculus of adapted monkeys. J Neurophysiol 43(5):1477–1493

    CAS  PubMed  Google Scholar 

  • Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299

    Article  CAS  PubMed  Google Scholar 

  • Mugnaini E (1983) The length of cerebellar parallel fibers in chicken and rhesus monkey. J Comp Neurol 220:7–15

    Article  CAS  PubMed  Google Scholar 

  • Murphy JT, Sabah NH (1971) Cerebellar Purkinje cell responses to afferent inputs. I. Climbing fiber activation. Brain Res 25(3):449–467

    Article  CAS  PubMed  Google Scholar 

  • Napper RMA, Harvey RJ (1988) Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J Comp Neurol 274:168–177

    Article  CAS  PubMed  Google Scholar 

  • Nelson WL (1983) Physical principles for economies of skilled movements. Biol Cybern 46(2):135–147

    Article  CAS  PubMed  Google Scholar 

  • Palkovits M, Magyar P, Szentagothai J (1972) Quantitative histological analysis of the cerebellar cortex in the cat. IV. Mossy fiber-Purkinje cell numerical transfer. Brain Res 45:15–29

    Article  CAS  PubMed  Google Scholar 

  • Palkovits M, Mezey E, Hamori J, Szentagothai J (1977) Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and on synapses. Exp Brain Res 28:189–209

  • Palmer C (1997) Music performance. Annu Rev Psychol 48:115–138. doi:10.1146/annurev.psych.48.1.115

  • Pedroarena CM, Schwarz C (2003) Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons. J Neurophysiol 89(2):704–715. doi:10.1152/jn.00558.2002

    Article  CAS  PubMed  Google Scholar 

  • Person AL, Raman IM (2012) Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature 481(7382):502–505. doi:10.1038/nature10732

    Article  CAS  Google Scholar 

  • Pichitpornchai C, Rawson JA, Rees S (1994) Morphology of parallel fibres in the cerebellar cortex of the rat: an experimental light and electron microscopic study with biocytin. J Comp Neurol 342:206–220

    Article  CAS  PubMed  Google Scholar 

  • Ramôn y Cajal S (1909) Histologie du Système Nerveux de l’Homme et des Vertébrés. Maloine, Paris

  • Ramôn y Cajal S (1911) Histologie du Système Nerveux de l’Homme et Vertébrés, vol 2. Maloine, Paris

  • Robinson DA (1981) The use of control systems analysis in the neurophysiology of eye movements. Annu Rev Neurosci 4:463–503. doi:10.1146/annurev.ne.04.030181.002335

  • Rossi F, Wiklund L, Van Der Want JJL, Strata P (1989) Climbing fibre plasticity in the cerebellum of the adult rat. Eur J Neurosci 1:543–547

    Article  PubMed  Google Scholar 

  • Schwartz EL (1977) Spatial mapping in the primate sensory projection: analytic structure and relevance to perception. Biol Cybern 25(4):181–194

    Article  CAS  PubMed  Google Scholar 

  • Schwartz EL (1980) A quantitative model of the functional architecture of human striate cortex with application to visual illusion and cortical texture analysis. Biol Cybern 37(2):63–76

    Article  CAS  PubMed  Google Scholar 

  • Shambes GM, Gibson JM, Welker W (1978) Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav Evol 15(2):94–140

    Article  CAS  PubMed  Google Scholar 

  • Shinoda Y, Sugihara I, Wu HS, Sugiuchi Y (2000) The entire trajectory of single climbing and mossy fibers in the cerebellar nuclei and cortex. Prog Brain Res 124:173–186

    Article  CAS  PubMed  Google Scholar 

  • Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 50:703–710

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stettler O, Joshi RL, Wizenmann A, Reingruber J, Holcman D, Bouillot C, Castagner F, Prochiantz A, Moya KL (2012) Engrailed homeoprotein recruits the adenosine A1 receptor to potentiate ephrin A5 function in retinal growth cones. Development 139(1):215–224. doi:10.1242/dev.063875

    Article  CAS  PubMed  Google Scholar 

  • Sugihara I, Fujita H, Na J, Quy PN, Li B-Y, Ikeda D (2009) Projection of reconstructed single purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. J Comp Neurol 512(2):282–304. doi:10.1002/cne.21889

    Article  CAS  PubMed  Google Scholar 

  • Sultan F (2000) Exploring a critical parameter of timing in the mouse cerebellar microcircuitry: the parallel fiber diameter. Neurosci Lett 280(1):41–44

    Article  CAS  PubMed  Google Scholar 

  • Sultan F (2001) Distribution of mossy fiber rosettes in the cerebellum of cats and mice: evidence for a parasagittal organization on the single fiber level. Eur J Neurosci 13(11):2123–2130

  • Sultan F, Braitenberg V (1993) Shapes and sizes of different mammalian cerebella. A study in quantitative comparative neuroanatomy. J Hirnforsch 34:79–92

  • Sultan F, Heck D (2003) Detection of sequences in the cerebellar cortex: numerical estimate of the possible number of tidal-wave inducing sequences represented. J Physiol Paris 97(4–6):591–600

    Article  CAS  PubMed  Google Scholar 

  • Thenozhi S, Yu W, Garrido R (2013) A novel numerical integrator for velocity and position estimation. Trans Inst Meas Control. doi:10.1177/0142331213476987

  • Voogd J (2004) Cerebellum and precerebellar nuclei. In: Paxinos G, May JK (eds) The human nervous system, vol 2. Elsevier, Amsterdam

    Google Scholar 

  • Waespe W, Henn V (1987) Gaze stabilization in the primate. Reviews of Physiology, Biochemistry and Pharmacology 106:37–125. doi:10.1007/BFb0027575

  • Wu HS, Sugihara I, Shinoda Y (1999) Projection patterns of single mossy fibers originating from the lateral reticular nucleus in the rat cerebellar cortex and nuclei. J Comp Neurol 411(1):97–118

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This paper was devised as a variation on a theme by Valentin Braitenberg (Braitenberg 1987). Braitenberg showed a rare combination of a translucent anatomist and a sharp theoretician. His scientific creativity probably first manifested itself in his seminal work on the cerebellar cortex’s anatomy (Braitenberg and Atwood 1958). Braitenberg always sought a functional interpretation of neuroanatomy and thought that theories should be instrumental in spurring experimental studies. He strongly believed that models of computing networks could be produced by consolidating top-down behavioral observations with bottom-up structural interpretations. I will always feel indebted to him for having mentored the early stages of my scientific pathway.

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  1. Department of Cognitive Neurology, Hertie Institute for Clinical Brain Research, Otfried-Müller-Str. 21, 72076 , Tübingen, Germany

    Fahad Sultan

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Correspondence to Fahad Sultan.

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This article forms part of a special issue of Biological Cybernetics entitled “Structural Aspects of Biological Cybernetics: Valentino Braitenberg, Neuroanatomy, and Brain Function”.

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Sultan, F. From cerebellar texture to movement optimization. Biol Cybern 108, 677–688 (2014). https://doi.org/10.1007/s00422-014-0618-2

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