Journal of Computational Neuroscience

, Volume 14, Issue 3, pp 311–327 | Cite as

No Parallel Fiber Volleys in the Cerebellar Cortex: Evidence from Cross-Correlation Analysis between Purkinje Cells in a Computer Model and in Recordings from Anesthetized Rats

  • Dieter Jaeger


Purkinje cells aligned on the medio-lateral axis share a large proportion of their ∼175,000 parallel fiber inputs. This arrangement has led to the hypothesis that movement timing is coded in the cerebellum by beams of synchronously active parallel fibers. In computer simulations I show that such synchronous activation leads to a narrow spike cross-correlation between pairs of Purkinje cells. This peak was completely absent when shared parallel fiber input was active in an asynchronous mode. To determine the presence of synchronous parallel fiber beams {in vivo} I recorded from pairs of Purkinje cells in crus IIa of anesthetized rats. I found a complete absence of precise spike synchronization, even when both cells were strongly modulated in their spike rate by trains of air-puff stimuli to the face. These results indicate that Purkinje cell spiking is not controlled by volleys of synchronous parallel fiber inputs in the conditions examined. Instead, the data support a model by which granule cells primarily control Purkinje cell spiking via dynamic population rate changes.

cerebellum temporal coding modeling rat in vivo excitation inhibition 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abeles M (1991) Corticonis: Neural Circuits of the Cerebral Cortex. Cambridge University Press, New York.Google Scholar
  2. Aertsen AM, Gerstein GL, Habib MK, Palm G (1989) Dynamics of neuronal firing correlation: Modulation of “effective connectivity”. J. Neurophysiol. 61: 900-917.PubMedGoogle Scholar
  3. Albus JS (1971) A theory of cerebellar function. Math. Biosci. 10: 25-61.CrossRefGoogle Scholar
  4. Barbour B (1993) Synaptic currents evoked in Purkinje cells by stimulating individual granule cells. Neuron. 11: 759-769.CrossRefPubMedGoogle Scholar
  5. Bell CC, Grimm RJ (1969) Discharge properties of Purkinje cells recorded on single and double microelectrodes. J. Neurophysiol. 32: 1044-1055.PubMedGoogle Scholar
  6. Bower JM (1997a) Control of sensory data acquisition. International Review of Neurobiology 41: 489-513.PubMedGoogle Scholar
  7. Bower JM (1997b) Is the cerebellum sensory for motor’s sake, or motor for sensory’s sake: The view from the whiskers of a rat? Prog. Brain. Res. 114: 483-516.Google Scholar
  8. Bower JM, Beeman D (1994) The Book of Genesis. Springer, New York.Google Scholar
  9. 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.PubMedGoogle Scholar
  10. Braitenberg V (1967) Is the cerebellar cortex a biological clock in the millisecond range? Prog. Brain. Res. 25: 334-346.PubMedGoogle Scholar
  11. Braitenberg V, Atwood RP (1958) Morphological observations on the cerebellar cortex. J. Comp. Neurol. 109: 1-33.PubMedGoogle Scholar
  12. 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: 229-277.PubMedGoogle Scholar
  13. Brody CD (1999) Correlations withouth synchrony. Neural Comp. 11: 1537-1551.CrossRefGoogle Scholar
  14. Cohen D, Yarom Y (1998) Patches of synchronized activity in the cerebellar cortex evoked by mossy-fiber stimulation: Questioning the role of parallel fibers. Proc. Natl. Acad. Sci. USA 95: 15032-15036.CrossRefPubMedGoogle Scholar
  15. Crepel F, Dhanjal SS, Garthwaite J (1981) Morphological and electrophysiological characteristics of rat cerebellar slices maintained in vitro. J. Physiol. (Lond.) 316: 127-138.Google Scholar
  16. De Schutter E (1998) Dendritic voltage and calcium-gated channels amplify the variability of postsynaptic responses in a Purkinje cell model. J. Neurophysiol. 80: 504-519.PubMedGoogle Scholar
  17. De Schutter E, Bower JM (1994a) An active membrane model of the cerebellar Purkinje cell I. Simulation of current clamp in slice. J. Neurophysiol. 71: 375-400.PubMedGoogle Scholar
  18. De Schutter E, Bower JM (1994b) An active membrane model of the cerebellar Purkinje cell. II. Simulation of synaptic responses. J. Neurophysiol. 71: 401-419.PubMedGoogle Scholar
  19. De Schutter E, Bower JM (1994c) Simulated responses of cerebellar Purkinje cells are independent of the dendritic location of granule cell synaptic inputs. Proc. Natl. Acad. Sci. USA 91: 4736-4740.PubMedGoogle Scholar
  20. Diesmann M, Gewaltig MO, Aertsen A (1999) Stable propagation of synchronous spiking in cortical neural networks. Nature 402: 529-533.CrossRefPubMedGoogle Scholar
  21. Dugas C, Smith AM (1992) Responses of cerebellar Purkinje cells to slip of a hand-held object. J. Neurophysiol. 67: 483-495.PubMedGoogle Scholar
  22. Ebner TJ, Bloedel JR (1981) Correlation between activity of Purkinje cells and its modification by natural peripheral stimuli. J. Neurophysiol. 45: 948-961.PubMedGoogle Scholar
  23. Eccles JC, Sasaki K, Strata P (1967) Interpretation of the field potentials generated in the cerebellar cortex by a mossy fibre volley. Exp. Brain Res. 3: 58-80.Google Scholar
  24. Fortier PA, Kalaska JF, Smith AM (1989) Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J. Neurophysiol. 62: 198-211.PubMedGoogle Scholar
  25. Garwicz M, Andersson G (1992) Spread of synaptic activity along parallel fibres in cat cerebellar anterior lobe. Exp. Brain Res. 88: 615-622.CrossRefPubMedGoogle Scholar
  26. Gauck V, Jaeger D (2000) The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J. Neurosci. 20: 3006-3016.PubMedGoogle Scholar
  27. Hartmann MJ, Bower JM (1998) Oscillatory activity in the cerebellar hemispheres of unrestrained rats. J. Neurophysiol. 80: 1598-1604.PubMedGoogle Scholar
  28. Hartmann MJ, Bower JM (2001) Tactile responses in the granule cell layer of cerebellar folium Crus IIa of freely behaving rats. J. Neurosci. 21: 3549-3563.PubMedGoogle Scholar
  29. Harvey RJ, Napper RMA (1991) Quantitative studies of the mammalian cerebellum. Prog. Neurobiol. 36: 437-463.CrossRefPubMedGoogle Scholar
  30. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19: 665-678.CrossRefPubMedGoogle Scholar
  31. Houk JC, Buckingham JT, Barto AG (1996) Models of the cerebellum and motor learning. Behav. Brain Sci. 19: 368-383.Google Scholar
  32. Huang C-M, Mu H, Hsiao C-F (1993) Identification of cell types from action potential waveforms: Cerebellar granule cells. Brain Res. 619: 313-318.CrossRefPubMedGoogle Scholar
  33. Isope P, Barbour P. (2001) The majority of granule cell Purkinje cell synapses are silent. Soc. Neurosci. Abstr. 27: Program No. 713.5.Google Scholar
  34. Ito M (1984) The Cerebellum and Neural Control. Raven Press, New York.Google Scholar
  35. Ivry R (1997) Cerebellar timing systems. Int. Rev. Neurobiol. 41: 555-573.PubMedGoogle Scholar
  36. Jaeger D, Bower JM (1994) Prolonged responses in rat cerebellar Purkinje cells following activation of the granule cell layer: An intracellular in vitro and in vivo investigation. Exp. Brain Res. 100: 200-214.CrossRefPubMedGoogle Scholar
  37. Jaeger D, Bower JM (1999) Synaptic control of spiking in cerebellar Purkinje cells: Dynamic current clamp based on model conductances. J. Neurosci 19: 6090-6101.PubMedGoogle Scholar
  38. Jaeger D, De Schutter E, Bower JM (1997) The role of synaptic and voltage-gated currents in the control of Purkinje cell spiking: A modeling study. J. Neurosci 17: 91-106.PubMedGoogle Scholar
  39. Johnson MJ, Alloway KD (1996) Cross-correlation analysis reveals laminar differences in thalamocortical interactions in the somatosensory system. J. Neurophysiol. 75: 1444-1457.PubMedGoogle Scholar
  40. Lang EJ, Sugihara I, Welsh JP, Llinás R (1999) Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. J. Neurosci. 19: 2728-2739.PubMedGoogle Scholar
  41. Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestiubloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J. Neurophysiol. 41: 733-763.PubMedGoogle Scholar
  42. Llinás R (1982) General discussion: Radial connectivity in the cerebellar cortex: A novel view regarding the functional organization of the molecular layer. In: SL Palay, V Chan-Palay, eds. The Cerebellum: New Vistas, (Exp. Brain Res. Suppl. Vol. 6). Springer Verlag, New York. pp. 189-194.Google Scholar
  43. Llinás R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. (Lond.) 305: 171-195.Google Scholar
  44. Mano N, Ito Y, Shibutani H (1991) Saccade-related Purkinje cells in the cerebellar hemispheres of the monkey. Exp. Brain Res. 84: 465-470.CrossRefPubMedGoogle Scholar
  45. Mano N-I, Yamamoto K-I (1980) Simple-spike activity of cerebellar Purkinje cells related to visually guided wrist tracking movement in the monkey. J. Neurophysiol. 43: 713-728.PubMedGoogle Scholar
  46. Mauk MD, Garcia KS, Medina JF, Steele PM (1998) Does cerebellar LTD mediate motor learning? Toward a resolution without a smoking gun. Neuron 20: 359-362.CrossRefPubMedGoogle Scholar
  47. Medina JF, Mauk MD (2000) Computer simulation of cerebellar information processing. Nat. Neurosci. 3: 1205-1211.CrossRefPubMedGoogle Scholar
  48. Moore GP, Segundo JP, Perkel DH, Levitan H (1970) Statistical signs of synaptic interaction in neurons. Biophys. J. 10: 876-900.PubMedGoogle Scholar
  49. 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.PubMedGoogle Scholar
  50. Palkovits M, Magyar P, Szentagothai J (1971) Quantitative histological analysis of the cerebellar cortex in the cat. III. Structural organization of the molecular layer. Brain Res. 34: 1-18.CrossRefPubMedGoogle Scholar
  51. Palm G, Aertsen AM, Gerstein GL (1988) On the significance of correlations among neuronal spike trains. Biol. Cybern. 59: 1-11.CrossRefPubMedGoogle Scholar
  52. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. II Simultaneous spike trains. Biophys. J. 7: 419-440.PubMedGoogle Scholar
  53. Rapp M, Yarom Y, Segev I (1992) The impact of parallel fiber background activity on the cable properties of cerebellar Purkinje cells. Neural Comput. 4: 518-533.Google Scholar
  54. Riehle A, Grün S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278: 1950-1953.CrossRefPubMedGoogle Scholar
  55. Santamaria F, Jaeger D, De Schutter E, Bower JM (2002) Modulatory effects of parallel fibers and stellate cell synaptic activity on Purkinje cell responses to ascending segment input: A modeling study. J. Comput. Neurosci. 13: 217-235.CrossRefPubMedGoogle Scholar
  56. Sasaki K, Strata P (1967) Responses evoked in the cerebellar cortex by stimulating mossy fibre pathways to the cerebellum. Experimental Brain Research 3: 95-110.CrossRefGoogle Scholar
  57. Savio T, Tempia F (1985) On the Purkinje cell activity increase induced by suppression of inferior olive activity. Exp. Brain Res. 57: 456-463.CrossRefPubMedGoogle Scholar
  58. Singer W (1999) Neuronal synchrony: A versatile code for the definition of relations? Neuron 24: 49-65.CrossRefPubMedGoogle Scholar
  59. Stratton SE, Lorden JF, Mays LE, Oltmans GA (1988) Spontaneous and harmaline-stimulated Purkinje cell activity in rats with a genetic movement disorder. J. Neurosci. 8: 3327-3336.PubMedGoogle Scholar
  60. Timmann D, Watts S, Hore J (1999) Failure of cerebellar patients to time finger opening precisely causes ball high-low inaccuracy in overarm throws. J. Neurophysiol. 82: 103-114.PubMedGoogle Scholar
  61. Vaadia E, Haalman I, Abeles M, Bergman YP, Slovin H, Aertsen A (1995) Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373: 515-518.CrossRefPubMedGoogle Scholar
  62. Welsh JP, Lang EJ, Sugihara I, LlinásR(1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374: 453-457.CrossRefPubMedGoogle Scholar
  63. Williams SR, Christensen SR, Stuart GJ, Hausser M (2002) Membrane potential bistability is controlled by the hyperpolarizationactivated current I(H) in rat cerebellar Purkinje neurons in vitro. J. Physiol 539: 469-483.CrossRefPubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Dieter Jaeger
    • 1
  1. 1.Department of BiologyEmory UniversityAtlantaUSA

Personalised recommendations