Skip to main content
Log in

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

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abeles M (1991) Corticonis: Neural Circuits of the Cerebral Cortex. Cambridge University Press, New York.

    Google Scholar 

  • Aertsen AM, Gerstein GL, Habib MK, Palm G (1989) Dynamics of neuronal firing correlation: Modulation of “effective connectivity”. J. Neurophysiol. 61: 900-917.

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Barbour B (1993) Synaptic currents evoked in Purkinje cells by stimulating individual granule cells. Neuron. 11: 759-769.

    Article  PubMed  Google Scholar 

  • Bell CC, Grimm RJ (1969) Discharge properties of Purkinje cells recorded on single and double microelectrodes. J. Neurophysiol. 32: 1044-1055.

    PubMed  Google Scholar 

  • Bower JM (1997a) Control of sensory data acquisition. International Review of Neurobiology 41: 489-513.

    PubMed  Google Scholar 

  • 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 

  • Bower JM, Beeman D (1994) The Book of Genesis. Springer, New York.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Braitenberg V (1967) Is the cerebellar cortex a biological clock in the millisecond range? Prog. Brain. Res. 25: 334-346.

    PubMed  Google Scholar 

  • Braitenberg V, Atwood RP (1958) Morphological observations on the cerebellar cortex. J. Comp. Neurol. 109: 1-33.

    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: 229-277.

    PubMed  Google Scholar 

  • Brody CD (1999) Correlations withouth synchrony. Neural Comp. 11: 1537-1551.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Diesmann M, Gewaltig MO, Aertsen A (1999) Stable propagation of synchronous spiking in cortical neural networks. Nature 402: 529-533.

    Article  PubMed  Google Scholar 

  • Dugas C, Smith AM (1992) Responses of cerebellar Purkinje cells to slip of a hand-held object. J. Neurophysiol. 67: 483-495.

    PubMed  Google Scholar 

  • Ebner TJ, Bloedel JR (1981) Correlation between activity of Purkinje cells and its modification by natural peripheral stimuli. J. Neurophysiol. 45: 948-961.

    PubMed  Google Scholar 

  • 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 

  • Fortier PA, Kalaska JF, Smith AM (1989) Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J. Neurophysiol. 62: 198-211.

    PubMed  Google Scholar 

  • Garwicz M, Andersson G (1992) Spread of synaptic activity along parallel fibres in cat cerebellar anterior lobe. Exp. Brain Res. 88: 615-622.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Hartmann MJ, Bower JM (1998) Oscillatory activity in the cerebellar hemispheres of unrestrained rats. J. Neurophysiol. 80: 1598-1604.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19: 665-678.

    Article  PubMed  Google Scholar 

  • Houk JC, Buckingham JT, Barto AG (1996) Models of the cerebellum and motor learning. Behav. Brain Sci. 19: 368-383.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Isope P, Barbour P. (2001) The majority of granule cell Purkinje cell synapses are silent. Soc. Neurosci. Abstr. 27: Program No. 713.5.

  • Ito M (1984) The Cerebellum and Neural Control. Raven Press, New York.

    Google Scholar 

  • Ivry R (1997) Cerebellar timing systems. Int. Rev. Neurobiol. 41: 555-573.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Johnson MJ, Alloway KD (1996) Cross-correlation analysis reveals laminar differences in thalamocortical interactions in the somatosensory system. J. Neurophysiol. 75: 1444-1457.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Mano N, Ito Y, Shibutani H (1991) Saccade-related Purkinje cells in the cerebellar hemispheres of the monkey. Exp. Brain Res. 84: 465-470.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Moore GP, Segundo JP, Perkel DH, Levitan H (1970) Statistical signs of synaptic interaction in neurons. Biophys. J. 10: 876-900.

    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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Palm G, Aertsen AM, Gerstein GL (1988) On the significance of correlations among neuronal spike trains. Biol. Cybern. 59: 1-11.

    Article  PubMed  Google Scholar 

  • Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. II Simultaneous spike trains. Biophys. J. 7: 419-440.

    PubMed  Google Scholar 

  • 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 

  • Riehle A, Grün S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278: 1950-1953.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Savio T, Tempia F (1985) On the Purkinje cell activity increase induced by suppression of inferior olive activity. Exp. Brain Res. 57: 456-463.

    Article  PubMed  Google Scholar 

  • Singer W (1999) Neuronal synchrony: A versatile code for the definition of relations? Neuron 24: 49-65.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Welsh JP, Lang EJ, Sugihara I, LlinásR(1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374: 453-457.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jaeger, D. 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. J Comput Neurosci 14, 311–327 (2003). https://doi.org/10.1023/A:1023217111784

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023217111784

Navigation