The detection and generation of sequences as a key to cerebellar function: Experiments and theory

V. Braitenberg, D. Heck, F. Sultan, M. A. Arbid, J. Spoelstra, J. G. Bjaalie, P. Brodal, J. M. Bower, G. A. Chauvet, E. Courchesne, M. Dufosse, A. Kaladjian, P. Grandguillaume, M. Garwiez, G. Andersson, J. S. Grethe, R. F. Thompson, R. J. Harvey, D. Jaeger, E. De SchutterE. E. Kadar, R. E. Shaw, M. T. Turvey, M. Lidierth, W. A. MacKay, G. McCollum, F. Mechsner, G. Palm, J. Meek, R. C. Miall, M. Molinari, L. Petrosini, P. Morasso, V. Sanguineti, M. G. Paulin, R. E. Poppele, G. Bosco, P. D. Roberts, C. Schwarz, R. E. Shaw, E. E. Kadar, M. T. Turvey, H. Topka, J. Dichgans, P. Trillenberg, K. Wessel, V. Braitenberg, D. Heck, F. Sultan

Research output: Contribution to journalArticle

182 Citations (Scopus)

Abstract

Starting from macroscopic and microscopic facts of cerebellar histology, we propose a new functional interpretation that may elucidate the role of the cerebellum in movement control. The idea is that the cerebellum is a large collection of individual lines (Eccles's 'beams': Eccles et al. 1967a) that respond specifically to certain sequences of events in the input and in turn produce sequences of signals in the output. We believe that the sequence- in/sequence-out modern of operation is as typical for the cerebellar cortex as the transformation of sets into sets of active neurons is typical for the cerebral cortex, and that both the histological differences between the two and their reciprocal functional interactions become understandable in the light of this dichotomy. The response of Purkinje cells to sequences of stimuli in the mossy fiber system was shown experimentally by Heek on surviving slices of rat and guinea pig cerebellum. Sequential activation of a row of eleven stimulating electrodes in the granular layer, imitating a 'movement of the stimuli along the folium, produces a powerful volley in the parallel fibers that strongly excites Purkinje cells, as evidenced by intracellular recording. The volley, or 'tidal wave,' has maximal amplitude when the stimulus moves toward the recording site at the speed of conduction in parallel fibers, and much smaller amplitudes for lower or higher 'velocities.' The succession of stimuli has no effect when they 'move' in the opposite direction. Synchronous activation of the stimulus electrodes also lind hardly any effect. We believe that the sequences of mossy fiber activation that normally produce this effect in the intact cerebellum are a combination of motor planning relayed to the cerebellum by the cerebral cortex, and information about ongoing movement, reaching the cerebellum from the spinal cord. The output elicited by the specific sequence to which a 'beam' is tuned may well be a succession of well timed inhibitory volleys 'sculpting' the motor sequences so as to adapt them to the complicated requirements of the physics of a multijointed system.

Original languageEnglish
Pages (from-to)229-277
Number of pages49
JournalBehavioral and Brain Sciences
Volume20
Issue number2
DOIs
Publication statusPublished - 1997

Fingerprint

cerebellum
Cerebellum
electrode
experiment
Purkinje Cells
cerebral cortex
Cerebral Cortex
electrodes
Tidal Waves
histology
Electrodes
pig
Cerebellar Cortex
physics
Physics
Protein Sorting Signals
signal peptide
spinal cord
guinea pigs
tides

Keywords

  • Allometric relation
  • Cerebellum
  • Cerebrocerebellar interaction
  • Motor control
  • Parallel fibers
  • Sequence addressable memory
  • Spatiotemporal activity
  • Synchronicity

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Neuroscience(all)
  • Psychology(all)
  • Neuropsychology and Physiological Psychology

Cite this

Braitenberg, V., Heck, D., Sultan, F., Arbid, M. A., Spoelstra, J., Bjaalie, J. G., ... Sultan, F. (1997). The detection and generation of sequences as a key to cerebellar function: Experiments and theory. Behavioral and Brain Sciences, 20(2), 229-277. https://doi.org/10.1017/S0140525X9700143X

The detection and generation of sequences as a key to cerebellar function : Experiments and theory. / Braitenberg, V.; Heck, D.; Sultan, F.; Arbid, M. A.; Spoelstra, J.; Bjaalie, J. G.; Brodal, P.; Bower, J. M.; Chauvet, G. A.; Courchesne, E.; Dufosse, M.; Kaladjian, A.; Grandguillaume, P.; Garwiez, M.; Andersson, G.; Grethe, J. S.; Thompson, R. F.; Harvey, R. J.; Jaeger, D.; De Schutter, E.; Kadar, E. E.; Shaw, R. E.; Turvey, M. T.; Lidierth, M.; MacKay, W. A.; McCollum, G.; Mechsner, F.; Palm, G.; Meek, J.; Miall, R. C.; Molinari, M.; Petrosini, L.; Morasso, P.; Sanguineti, V.; Paulin, M. G.; Poppele, R. E.; Bosco, G.; Roberts, P. D.; Schwarz, C.; Shaw, R. E.; Kadar, E. E.; Turvey, M. T.; Topka, H.; Dichgans, J.; Trillenberg, P.; Wessel, K.; Braitenberg, V.; Heck, D.; Sultan, F.

In: Behavioral and Brain Sciences, Vol. 20, No. 2, 1997, p. 229-277.

Research output: Contribution to journalArticle

Braitenberg, V, Heck, D, Sultan, F, Arbid, MA, Spoelstra, J, Bjaalie, JG, Brodal, P, Bower, JM, Chauvet, GA, Courchesne, E, Dufosse, M, Kaladjian, A, Grandguillaume, P, Garwiez, M, Andersson, G, Grethe, JS, Thompson, RF, Harvey, RJ, Jaeger, D, De Schutter, E, Kadar, EE, Shaw, RE, Turvey, MT, Lidierth, M, MacKay, WA, McCollum, G, Mechsner, F, Palm, G, Meek, J, Miall, RC, Molinari, M, Petrosini, L, Morasso, P, Sanguineti, V, Paulin, MG, Poppele, RE, Bosco, G, Roberts, PD, Schwarz, C, Shaw, RE, Kadar, EE, Turvey, MT, Topka, H, Dichgans, J, Trillenberg, P, Wessel, K, Braitenberg, V, Heck, D & Sultan, F 1997, 'The detection and generation of sequences as a key to cerebellar function: Experiments and theory', Behavioral and Brain Sciences, vol. 20, no. 2, pp. 229-277. https://doi.org/10.1017/S0140525X9700143X
Braitenberg, V. ; Heck, D. ; Sultan, F. ; Arbid, M. A. ; Spoelstra, J. ; Bjaalie, J. G. ; Brodal, P. ; Bower, J. M. ; Chauvet, G. A. ; Courchesne, E. ; Dufosse, M. ; Kaladjian, A. ; Grandguillaume, P. ; Garwiez, M. ; Andersson, G. ; Grethe, J. S. ; Thompson, R. F. ; Harvey, R. J. ; Jaeger, D. ; De Schutter, E. ; Kadar, E. E. ; Shaw, R. E. ; Turvey, M. T. ; Lidierth, M. ; MacKay, W. A. ; McCollum, G. ; Mechsner, F. ; Palm, G. ; Meek, J. ; Miall, R. C. ; Molinari, M. ; Petrosini, L. ; Morasso, P. ; Sanguineti, V. ; Paulin, M. G. ; Poppele, R. E. ; Bosco, G. ; Roberts, P. D. ; Schwarz, C. ; Shaw, R. E. ; Kadar, E. E. ; Turvey, M. T. ; Topka, H. ; Dichgans, J. ; Trillenberg, P. ; Wessel, K. ; Braitenberg, V. ; Heck, D. ; Sultan, F. / The detection and generation of sequences as a key to cerebellar function : Experiments and theory. In: Behavioral and Brain Sciences. 1997 ; Vol. 20, No. 2. pp. 229-277.
@article{41eae201d308434ca8319c3c09e645a9,
title = "The detection and generation of sequences as a key to cerebellar function: Experiments and theory",
abstract = "Starting from macroscopic and microscopic facts of cerebellar histology, we propose a new functional interpretation that may elucidate the role of the cerebellum in movement control. The idea is that the cerebellum is a large collection of individual lines (Eccles's 'beams': Eccles et al. 1967a) that respond specifically to certain sequences of events in the input and in turn produce sequences of signals in the output. We believe that the sequence- in/sequence-out modern of operation is as typical for the cerebellar cortex as the transformation of sets into sets of active neurons is typical for the cerebral cortex, and that both the histological differences between the two and their reciprocal functional interactions become understandable in the light of this dichotomy. The response of Purkinje cells to sequences of stimuli in the mossy fiber system was shown experimentally by Heek on surviving slices of rat and guinea pig cerebellum. Sequential activation of a row of eleven stimulating electrodes in the granular layer, imitating a 'movement of the stimuli along the folium, produces a powerful volley in the parallel fibers that strongly excites Purkinje cells, as evidenced by intracellular recording. The volley, or 'tidal wave,' has maximal amplitude when the stimulus moves toward the recording site at the speed of conduction in parallel fibers, and much smaller amplitudes for lower or higher 'velocities.' The succession of stimuli has no effect when they 'move' in the opposite direction. Synchronous activation of the stimulus electrodes also lind hardly any effect. We believe that the sequences of mossy fiber activation that normally produce this effect in the intact cerebellum are a combination of motor planning relayed to the cerebellum by the cerebral cortex, and information about ongoing movement, reaching the cerebellum from the spinal cord. The output elicited by the specific sequence to which a 'beam' is tuned may well be a succession of well timed inhibitory volleys 'sculpting' the motor sequences so as to adapt them to the complicated requirements of the physics of a multijointed system.",
keywords = "Allometric relation, Cerebellum, Cerebrocerebellar interaction, Motor control, Parallel fibers, Sequence addressable memory, Spatiotemporal activity, Synchronicity",
author = "V. Braitenberg and D. Heck and F. Sultan and Arbid, {M. A.} and J. Spoelstra and Bjaalie, {J. G.} and P. Brodal and Bower, {J. M.} and Chauvet, {G. A.} and E. Courchesne and M. Dufosse and A. Kaladjian and P. Grandguillaume and M. Garwiez and G. Andersson and Grethe, {J. S.} and Thompson, {R. F.} and Harvey, {R. J.} and D. Jaeger and {De Schutter}, E. and Kadar, {E. E.} and Shaw, {R. E.} and Turvey, {M. T.} and M. Lidierth and MacKay, {W. A.} and G. McCollum and F. Mechsner and G. Palm and J. Meek and Miall, {R. C.} and M. Molinari and L. Petrosini and P. Morasso and V. Sanguineti and Paulin, {M. G.} and Poppele, {R. E.} and G. Bosco and Roberts, {P. D.} and C. Schwarz and Shaw, {R. E.} and Kadar, {E. E.} and Turvey, {M. T.} and H. Topka and J. Dichgans and P. Trillenberg and K. Wessel and V. Braitenberg and D. Heck and F. Sultan",
year = "1997",
doi = "10.1017/S0140525X9700143X",
language = "English",
volume = "20",
pages = "229--277",
journal = "Behavioral and Brain Sciences",
issn = "0140-525X",
publisher = "Cambridge University Press",
number = "2",

}

TY - JOUR

T1 - The detection and generation of sequences as a key to cerebellar function

T2 - Experiments and theory

AU - Braitenberg, V.

AU - Heck, D.

AU - Sultan, F.

AU - Arbid, M. A.

AU - Spoelstra, J.

AU - Bjaalie, J. G.

AU - Brodal, P.

AU - Bower, J. M.

AU - Chauvet, G. A.

AU - Courchesne, E.

AU - Dufosse, M.

AU - Kaladjian, A.

AU - Grandguillaume, P.

AU - Garwiez, M.

AU - Andersson, G.

AU - Grethe, J. S.

AU - Thompson, R. F.

AU - Harvey, R. J.

AU - Jaeger, D.

AU - De Schutter, E.

AU - Kadar, E. E.

AU - Shaw, R. E.

AU - Turvey, M. T.

AU - Lidierth, M.

AU - MacKay, W. A.

AU - McCollum, G.

AU - Mechsner, F.

AU - Palm, G.

AU - Meek, J.

AU - Miall, R. C.

AU - Molinari, M.

AU - Petrosini, L.

AU - Morasso, P.

AU - Sanguineti, V.

AU - Paulin, M. G.

AU - Poppele, R. E.

AU - Bosco, G.

AU - Roberts, P. D.

AU - Schwarz, C.

AU - Shaw, R. E.

AU - Kadar, E. E.

AU - Turvey, M. T.

AU - Topka, H.

AU - Dichgans, J.

AU - Trillenberg, P.

AU - Wessel, K.

AU - Braitenberg, V.

AU - Heck, D.

AU - Sultan, F.

PY - 1997

Y1 - 1997

N2 - Starting from macroscopic and microscopic facts of cerebellar histology, we propose a new functional interpretation that may elucidate the role of the cerebellum in movement control. The idea is that the cerebellum is a large collection of individual lines (Eccles's 'beams': Eccles et al. 1967a) that respond specifically to certain sequences of events in the input and in turn produce sequences of signals in the output. We believe that the sequence- in/sequence-out modern of operation is as typical for the cerebellar cortex as the transformation of sets into sets of active neurons is typical for the cerebral cortex, and that both the histological differences between the two and their reciprocal functional interactions become understandable in the light of this dichotomy. The response of Purkinje cells to sequences of stimuli in the mossy fiber system was shown experimentally by Heek on surviving slices of rat and guinea pig cerebellum. Sequential activation of a row of eleven stimulating electrodes in the granular layer, imitating a 'movement of the stimuli along the folium, produces a powerful volley in the parallel fibers that strongly excites Purkinje cells, as evidenced by intracellular recording. The volley, or 'tidal wave,' has maximal amplitude when the stimulus moves toward the recording site at the speed of conduction in parallel fibers, and much smaller amplitudes for lower or higher 'velocities.' The succession of stimuli has no effect when they 'move' in the opposite direction. Synchronous activation of the stimulus electrodes also lind hardly any effect. We believe that the sequences of mossy fiber activation that normally produce this effect in the intact cerebellum are a combination of motor planning relayed to the cerebellum by the cerebral cortex, and information about ongoing movement, reaching the cerebellum from the spinal cord. The output elicited by the specific sequence to which a 'beam' is tuned may well be a succession of well timed inhibitory volleys 'sculpting' the motor sequences so as to adapt them to the complicated requirements of the physics of a multijointed system.

AB - Starting from macroscopic and microscopic facts of cerebellar histology, we propose a new functional interpretation that may elucidate the role of the cerebellum in movement control. The idea is that the cerebellum is a large collection of individual lines (Eccles's 'beams': Eccles et al. 1967a) that respond specifically to certain sequences of events in the input and in turn produce sequences of signals in the output. We believe that the sequence- in/sequence-out modern of operation is as typical for the cerebellar cortex as the transformation of sets into sets of active neurons is typical for the cerebral cortex, and that both the histological differences between the two and their reciprocal functional interactions become understandable in the light of this dichotomy. The response of Purkinje cells to sequences of stimuli in the mossy fiber system was shown experimentally by Heek on surviving slices of rat and guinea pig cerebellum. Sequential activation of a row of eleven stimulating electrodes in the granular layer, imitating a 'movement of the stimuli along the folium, produces a powerful volley in the parallel fibers that strongly excites Purkinje cells, as evidenced by intracellular recording. The volley, or 'tidal wave,' has maximal amplitude when the stimulus moves toward the recording site at the speed of conduction in parallel fibers, and much smaller amplitudes for lower or higher 'velocities.' The succession of stimuli has no effect when they 'move' in the opposite direction. Synchronous activation of the stimulus electrodes also lind hardly any effect. We believe that the sequences of mossy fiber activation that normally produce this effect in the intact cerebellum are a combination of motor planning relayed to the cerebellum by the cerebral cortex, and information about ongoing movement, reaching the cerebellum from the spinal cord. The output elicited by the specific sequence to which a 'beam' is tuned may well be a succession of well timed inhibitory volleys 'sculpting' the motor sequences so as to adapt them to the complicated requirements of the physics of a multijointed system.

KW - Allometric relation

KW - Cerebellum

KW - Cerebrocerebellar interaction

KW - Motor control

KW - Parallel fibers

KW - Sequence addressable memory

KW - Spatiotemporal activity

KW - Synchronicity

UR - http://www.scopus.com/inward/record.url?scp=0031465549&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0031465549&partnerID=8YFLogxK

U2 - 10.1017/S0140525X9700143X

DO - 10.1017/S0140525X9700143X

M3 - Article

C2 - 10096998

AN - SCOPUS:0031465549

VL - 20

SP - 229

EP - 277

JO - Behavioral and Brain Sciences

JF - Behavioral and Brain Sciences

SN - 0140-525X

IS - 2

ER -