An adaptive filter model of cerebellar zone C3 as a basis for safe limb control?

Journal of Physiology

Volumn 591, Issue 22, 2013, Pages 5459-5474

  Dean, Paul ^a   Anderson, Sean ^a   Porrill, John ^a   Jörntell, Henrik ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE FILTER MODEL; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; CEREBELLAR ZONE C3; CEREBELLUM; HUMAN; INTERNEURON; MATHEMATICAL MODEL; MOTOR CONTROL; MOTOR COORDINATION; NERVE CELL PLASTICITY; NOCICEPTION; NOISE REDUCTION; NONHUMAN; PRIORITY JOURNAL; RECEPTIVE FIELD; ROBOTICS; WITHDRAWAL REFLEX;

ANIMALS; CEREBELLAR CORTEX; CEREBELLUM; EXTREMITIES; HUMANS; MODELS, NEUROLOGICAL; MOVEMENT; NERVE NET; REFLEX, VESTIBULO-OCULAR; SYNAPSES;

EID: 84887609584     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.261545     Document Type: Article

References (95)

1. Abrahamsson T, Cathala L, Matsui K, Shigemoto R & DiGregorio DA (2012). Thin dendrites of cerebellar interneurons confer sublinear synaptic integration and a gradient of short-term plasticity. Neuron 73, 1159-1172.
2. Albus JS (1971). A theory of cerebellar function. Math Biosci 10, 25-61.
3. Anderson SR, Pearson MJ, Pipe A, Prescott T, Dean P & Porrill J (2010). Adaptive cancelation of self-generated sensory signals in a whisking robot. IEEE Trans Robot 26, 1065-1076.
4. Anderson SR, Porrill J, Pearson MJ, Pipe A, Prescott T & Dean P (2012). An internal model architecture for novelty detection: Implications for cerebellar and collicular roles in sensory processing. PLoS ONE 7, e44560.
5. Apps R & Garwicz M (2005). Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6, 297-311.
6. Apps R & Lee S (2002). Central regulation of cerebellar climbing fibre input during motor learning. J Physiol 541, 301-317.
7. Arenz A, Bracey EF & Margrie TW (2009). Sensory representations in cerebellar granule cells. Curr Opin Neurobiol 19, 445-451.
8. Bell CC, Han V & Sawtell NB (2008). Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31, 1-24.
9. Bengtsson F & Jörntell H (2009). Sensory transmission in cerebellar granule cells relies on similarly coded mossy fiber inputs. Proc Natl Acad Sci U S A 106, 2389-2394.
10. Blakemore SJ, Wolpert D & Frith C (1999). The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation. Neuroimage 10, 448-459.
11. Bracha V, Kolb FP, Irwin KB & Bloedel JR (1999). Inactivation of interposed nuclei in the cat: classically conditioned withdrawal reflexes, voluntary limb movements and the action primitive hypothesis. Exp Brain Res 126, 77-92.
12. Carey MR (2011). Synaptic mechanisms of sensorimotor learning in the cerebellum. Curr Opin Neurobiol 21, 609-615.
13. Chadderton PT, Margrie TW & Hausser M (2004). Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860.
14. Clendenin M, Ekerot CF, Oscarsson O & Rosen I (1974). The lateral reticular nucleus in the cat. I. Mossy fibre distribution in cerebellar cortex. Exp Brain Res 21, 473-486.
15. Consalez GG & Hawkes R (2013). The compartmental restriction of cerebellar interneurons. Front Neural Circuits 6, Article 123.
16. D'Angelo E (2011). Neural circuits of the cerebellum: hypothesis for function. J Integr Neurosci 10, 317-352.
17. D'Angelo E & De Zeeuw CI (2009). Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci 32, 30-40.
18. D'Angelo E, Koekkoek SK, Lombardo P, Solinas S, Ros E, Garrido J, Schonewille M & De Zeeuw CI (2009). Timing in the cerebellum: oscillations and resonance in the granular layer. Neuroscience 162, 805-815.
19. D'Angelo E, Mazzarello P, Prestori F, Mapelli J, Solinas S, Lombardo P, Cesana E, Gandolfi D & Congi L (2011). The cerebellar network: From structure to function and dynamics. Brain Res Rev 66, 5-15.
20. De Zeeuw CI & Yeo CH (2005). Time and tide in cerebellar memory formation. Curr Opin Neurobiol 15, 667-674.
21. Dean P & Porrill J (2010). The cerebellum as an adaptive filter: a general model Funct Neurol 25, 1-8.
22. Dean P & Porrill J (2011). Evaluating the adaptive-filter model of the cerebellum. J Physiol 589, 3459-3470.
23. Dean P, Porrill J & Stone JV (2002). Decorrelation control by the cerebellum achieves oculomotor plant compensation in simulated vestibulo-ocular reflex. Proc R Soc Lond B Biol Sci 269, 1895-1904.
24. Dean P, Porrill J, Ekerot CF & Jörntell H (2010). The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat Rev Neurosci 11, 30-43.
25. Dizon MJ & Khodakhah K (2011). The role of interneurons in shaping Purkinje cell responses in the cerebellar cortex. J Neurosci 31, 10463-10473.
26. Edin B (2001). Cutaneous afferents provide information about knee joint movements in humans. J Physiol 531, 289-297.
27. Edin BB & Johansson N (1995). Skin strain patterns provide kinaesthetic information to the human central nervous system. J Physiol 487( Pt 1 ), 243-251.
28. Ekerot CF & Jörntell H (2001). Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. Eur J Neurosci 13, 1303-1310.
29. Ekerot CF & Jörntell H (2003). Parallel fiber receptive fields: a key to understanding cerebellar operation and learning. Cerebellum 2, 101-109.
30. Ekerot CF & Jörntell H (2008). Synaptic integration in cerebellar granule cells. Cerebellum 7, 539-541.
31. Ekerot CF, Garwicz M & Schouenborg J (1991a). The postsynaptic dorsal column pathway mediates cutaneous nociceptive information to cerebellar climbing fibres in the cat. J Physiol 441, 275-284.
32. Ekerot CF, Garwicz M & Schouenborg J (1991b). Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. J Physiol 441, 257-274.
33. Ekerot C-F, Jörntell H & Garwicz M (1995). Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat. Exp Brain Res 106, 365-376.
34. Fujita M (1982). Adaptive filter model of the cerebellum. Biol Cybern 45, 195-206.
35. Galliano E, Mazzarello P & D'Angelo E (2010). Discovery and rediscoveries of Golgi cells. J Physiol 588, 3639-3655.
36. Gao ZY, van Beugen BJ & De Zeeuw CI (2012). Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci 13, 619-635.
37. Garwicz M, Jörntell H & Ekerot CF (1998). Cutaneous receptive fields and topography of mossy fibres and climbing fibres projecting to cat cerebellar C3 zone. J Physiol 512( Pt 1 ), 277-293.
38. Garwicz M, Levinsson A & Schouenborg J (2002). Common principles of sensory encoding in spinal reflex modules and cerebellar climbing fibres. J Physiol 540, 1061-1069.
39. Gibson AR, Robinson FR, Alam J & Houk JC (1987). Somatotopic alignment between climbing fiber input and nuclear output of the cat intermediate cerebellum. J Comp Neurol 260, 362-377.
40. Gomi H & Kawato M (1993). Neural network control for a closed-loop system using feedback-error-learning. Neural Netw 6, 933-946.
41. Herculano-Houzel S (2009). The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci 3, 31.
42. Herreros I & Verschure PFMJ (2013). Nucleo-olivary inhibition balances the interaction between the reactive and adaptive layers in motor control. Neural Netw, doi.org/10.1016/j.neunet.2013.01.026.
43. Herrick CJ (1924). Origin and evolution of the cerebellum. Arch Neurol Psychiatry 11, 621-652.
44. Horn KM, Pong M & Gibson AR (2010). Functional relations of cerebellar modules of the cat. J Neurosci 30, 9411-9423.
45. Ito M (1970). Neurophysiological aspects of the cerebellar motor control system. Int J Neurol 7, 162-176.
46. Ito M (1984). The Cerebellum and Neural Control. Raven Press, New York.
47. Ito M (1997). Cerebellar microcomplexes. Int Rev Neurobiol 41, 475-487.
48. Jankowska E (1992). Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38, 335-378.
49. Jörntell H & Ekerot C-F (1999). Topographical organization of projections to cat motor cortex from nucleus interpositus anterior and forelimb skin. J Physiol 514, 551-566.
50. Jörntell H & Ekerot CF (2002). Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34, 797-806.
51. Jörntell H & Ekerot CF (2003). Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. J Neurosci 23, 9620-9631.
52. Jörntell H & Ekerot CF (2006). Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci 26, 11786-11797.
53. Jörntell H & Ekerot CF (2011). Receptive field remodeling induced by skin stimulation in cerebellar neurons in vivo. Front Neural Circuits 5, Article 3.
54. Jörntell H & Hansel C (2006). Synaptic memories upside down: bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron 52, 227-238.
55. Jörntell H, Garwicz M & Ekerot CF (1996). Relation between cutaneous receptive fields and muscle afferent input to climbing fibres projecting to the cerebellar C3 zone in the cat. Eur J Neurosci 8, 1769-1779.
56. Jörntell H, Bengtsson F, Schonewille M & De Zeeuw CI (2010). Cerebellar molecular layer interneurons - computational properties and roles in learning. Trends Neurosci 33, 524-532.
57. Kawato M (1990). Feedback-error-learning neural network for supervised motor learning. In Advanced Neural Computers, ed. Eckmiller R, pp. 365-372. Elsevier, Amsterdam.
58. Kitazawa S, Ohki Y, Sasaki M, Xi M & Hongo T (1993). Candidate premotor neurons of skin reflex pathways to T1 forelimb motoneurons of the cat. Exp Brain Res 95, 291-307.
59. Kolb FP, Irwin KB, Bloedel JR & Bracha V (1997). Conditioned and unconditioned forelimb reflex systems in the cat: involvement of the intermediate cerebellum. Exp Brain Res 114, 255-270.
60. Lenz A, Balakrishnan T, Pipe AG & Melhuish C (2008). An adaptive gaze stabilization controller inspired by the vestibulo-ocular reflex. Bioinspir Biomim 3, 035001.
61. Lenz A, Anderson SR, Pipe AG, Melhuish C, Dean P & Porrill J (2009). Cerebellar inspired adaptive control of a compliant robot actuated by pneumatic artificial muscles. IEEE Trans Syst Man Cybern B Cybern 39, 1420-1433.
62. Lepora N, Porrill J, Yeo CH & Dean P (2010). Sensory prediction or motor control? Application of Marr-Albus models of cerebellar function to classical conditioning. Front Comput Neurosci 4, 1-16.
63. Marr D (1969). A theory of cerebellar cortex. J Physiol 202, 437-470.
64. Mathews PJ, Lee KH, Peng ZC, Houser CR & Otis TS (2012). Effects of climbing fiber driven inhibition on Purkinje neuron spiking. J Neurosci 32, 17988-17997.
65. 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, 5516-5525.
66. Miall RC & Wolpert DM (1996). Forward models for physiological motor control. Neural Netw 9, 1265-1279.
67. Mostofi A, Holtzman T, Grout AS, Yeo CH & Edgley SA (2010). Electrophysiological localization of eyeblink-related microzones in rabbit cerebellar cortex. J Neurosci 30, 8920-8934.
68. Ohtsuki G, Piochon C & Hansel C (2009). Climbing fiber signaling and cerebellar gain control. Front Cell Neurosci 3, Article 4.
69. Oscarsson O (1980). Functional organization of olivary projection to the cerebellar anterior lobe. In The inferior olivary nucleus: Anatomy and physiology, ed. Courville J, de Montigney C & Lamarre Y, pp. 279-289. Raven Press, New York.
70. Park SM, Tara E & Khodakhah K (2012). Efficient generation of reciprocal signals by inhibition. J Neurophysiol 107, 2453-2462.
71. Pijpers A, Apps R, Pardoe J, Voogd J & Ruigrok TJH (2006). Precise spatial relationships between mossy fibers and climbing fibers in rat cerebellar cortical zones. J Neurosci 26, 12067-12080.
72. Pijpers A, Winkelman BHJ, Bronsing R & Ruigrok TJH (2008). Selective impairment of the cerebellar C1 module involved in rat hind limb control reduces step-dependent modulation of cutaneous reflexes. J Neurosci 28, 2179-2189.
73. Porrill J & Dean P (2008). Silent synapses, LTP and the indirect parallel-fibre pathway: computational consequences of optimal noise processing. PLoS Comput Biol 4, e1000085.
74. Porrill J, Dean P & Stone JV (2004). Recurrent cerebellar architecture solves the motor error problem. Proc R Soc Lond B Biol Sci 271, 789-796.
75. Porrill J, Dean P & Anderson SR (2013). Adaptive filters and internal models: Multilevel description of cerebellar function. Neural Netw, doi.org/10.1016/j.neunet2012.12.005.
76. Raphael G, Tsianos GA & Loeb GE (2010). Spinal-like regulator facilitates control of a two-degree-of-freedom wrist. J Neurosci 30, 9431-9444.
77. Raymond JL, Lisberger SG & Mauk MD (1996). The cerebellum: a neuronal learning machine Science 272, 1126-1131.
78. Rotto DM & Kaufman MP (1988). Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol 64, 2306-2313.
79. Rybicki KJ, Waldrop TG & Kaufman MP (1985). Increasing gracilis muscle interstitial potassium concentrations stimulate group III and IV afferents. J Appl Physiol 58, 936-941.
80. Schouenborg J, Weng HR, Kalliomaki J & Holmberg H (1995). A survey of spinal dorsal horn neurones encoding the spatial organization of withdrawal reflexes in the rat. Exp Brain Res 106, 19-27.
81. Sejnowski TJ (1977). Storing covariance with nonlinearly interacting neurons. J Math Biol 4, 303-321.
82. Spanne A & Jörntell H (2013). Processing of multi-dimensional sensorimotor information in the spinal and cerebellar neurnal circuitry: a new hypothesis. PLoS Comput Biol 9, e1002979.
83. Timmann D, Kolb FP, Baier C, Rijntjes M, Muller SP, Diener HC & Weiller C (1996). Cerebellar activation during classical conditioning of the human flexion reflex: A PET study. Neuroreport 7, 2056-2060.
84. Timmann D, Baier PC, Diener HC & Kolb FP (2000). Classically conditioned withdrawal reflex in cerebellar patients 1. Impaired conditioned responses. Exp Brain Res 130, 453-470.
85. Trivedi D, Rahn CD, Kier WM & Walker ID (2008). Soft robotics: Biological inspiration, state of the art, and future research. Appl Bionics Biomech 5, 99-117.
86. Tyrrell T & Willshaw D (1992). Cerebellar cortex: its simulation and the relevance of Marr's theory. Philos Trans R Soc Lond B Biol Sci 336, 239-257.
87. Van Kan PLE, Gibson AR & Houk JC (1993a). Movement-related inputs to intermediate cerebellum of the monkey. J Neurophysiol 69, 74-94.
88. Van Kan PLE, Houk JC & Gibson AR (1993b). Output organization of intermediate cerebellum of the monkey. J Neurophysiol 69, 57-73.
89. Voogd J & Bigare F (1980). Topographical distribution of olivary and cortico nuclear fibers in the cerebellum a review. In The Inferior Olivary Nucleus: Anatomy and Physiology, ed. Courville J, De Montigny C & Lamarre Y, pp. 207-234. Raven Press, New York, N.Y.
90. Widrow B & Stearns SD (1985). Adaptive Signal Processing. Prentice-Hall Inc, Engelwood Cliffs, NJ.
91. Widrow B, Glover JR, Mccool JM, Kaunitz J, Williams CS, Hearn RH, Zeidler JR, Dong E & Goodlin RC (1975). Adaptive noise cancelling - principles and applications. Proc IEEE 63, 1692-1716.
92. Wiesendanger R & Wiesendanger M (1987). Topography of the corticofugal projection to the lateral reticular nucleus in the monkey. J Comp Neurol 256, 570-580.
93. Wolpert DM, Miall RC & Kawato M (1998). Internal models in the cerebellum. Trends Cog Sci 2, 338-347.
94. Yamazaki T & Tanaka S (2009). Computational models of timing mechanisms in the cerebellar granular layer. Cerebellum 8, 423-432.
95. Yeo CH & Hesslow G (1998). Cerebellum and conditioned reflexes. Trends Cog Sci 2, 322-330.