Key Points
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The olivocerebellar system is organized in modules and the cerebellar cortex is organized in Purkinje cell zones with common climbing-fibre inputs.
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Neurons in the inferior olive are electrotonically coupled, and as a consequence the complex spikes of Purkinje cells have a tendency to occur in synchrony.
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Neurons in the inferior olive show subthreshold oscillations and as a consequence the complex spikes of Purkinje cells have a tendency to occur rhythmically and to occur at specific time points.
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Simple spikes can also show spatiotemporal patterns in that they can also occur in synchrony and in short regular patterns, which can be triggered by sensorimotor stimulation.
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The simple-spike patterns and their intervals result from the intrinsic activity of Purkinje cells and their excitatory and inhibitory synaptic inputs, which are all subject to plastic processes.
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The impact of complex-spike activity on simple-spike activity can be divided in acute natural impacts, heterosynaptic plasticity and global inhibition, all of which can have an impact on motor behaviour.
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In many mouse mutants, changes in spatiotemporal patterns of Purkinje cell activity can be correlated with some deficit in motor performance, motor learning or motor consolidation.
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The cerebellar nuclei are sensitive to synchronous Purkinje cell input.
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Synchronous Purkinje cell input may result in rebound firing in cerebellar nucleus neurons.
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The mossy- and climbing-fibre collaterals that impinge on cerebellar nuclei can undergo plasticity that is dependent on Purkinje cell input.
Abstract
Neurons are generally considered to communicate information by increasing or decreasing their firing rate. However, in principle, they could in addition convey messages by using specific spatiotemporal patterns of spiking activities and silent intervals. Here, we review expanding lines of evidence that such spatiotemporal coding occurs in the cerebellum, and that the olivocerebellar system is optimally designed to generate and employ precise patterns of complex spikes and simple spikes during the acquisition and consolidation of motor skills. These spatiotemporal patterns may complement rate coding, thus enabling precise control of motor and cognitive processing at a high spatiotemporal resolution by fine-tuning sensorimotor integration and coordination.
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Acknowledgements
We kindly thank the following organizations for their financial support: the Netherlands Organization for Medical Sciences (ZonMw) to C.I.D.Z., the Netherlands Organization for Life Sciences (ALW) to C.I.D.Z., F.E.H., M.S. and S.K.K., Fonds Economische Stuurversterking (NeuroBasic project) to C.I.D.Z., the Erasmus University Fellowship to F.E.H. and M.S., the Prinses Beatrix Fonds to C.I.D.Z., and the SENSOPAC (sensorimotor structuring of perception and action for emergent cognition), CEREBNET and C7 programs of the European Community to C.I.D.Z. We also thank our laboratory members for valuable discussions.
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Glossary
- Convergence ratio
-
The ratio of input cells versus output cells — for example, many Purkinje cells of the same microzone project to the same target neuron in the cerebellar nuclei, resulting in a high ratio.
- Vestibulocerebellum
-
Part of the cerebellum (including the flocculus, nodulus and uvula) that controls compensatory eye and head movements.
- Zone
-
A sagittal region of Purkinje cells in the cerebellar cortex that is up to 500 μm wide and that receives climbing fibres from a particular olivary subnucleus.
- Microzone
-
A sagittal region of Purkinje cells within a cerebellar zone that is approximately 50 to 100 μm wide, that can be activated by a particular functional stimulus and that receives climbing fibres from a cluster of coupled olivary neurons.
- Leakage current
-
Electrical current that is induced by synaptic afferents (for example, at olivary spines) that affects the efficiency of gap junction coupling between these spines.
- Jitter
-
A measure for noise in spiking activities.
- Patch
-
A group of Purkinje cells characterized by a common response to a particular mossy fibre input, and that covers a small irregular area rather than a parallel beam or sagittal zone.
- Optokinetic reflex
-
Compensatory eye movements following visual whole-field stimulation.
- Crus 2
-
Part of the cerebellar hemisphere immediately rostral to the paramedian lobule.
- Paramedian lobule
-
Part of the cerebellar hemisphere immediately caudal to Crus 2.
- CV2 value
-
Coefficient of variation for adjacent interspike intervals.
- Downstate
-
The state of a cell in which the membrane potential is low and hardly any spikes are fired.
- Upstate
-
The state of a cell in which the membrane potential is normal or high, and spikes are fired.
- Rebound potentiation
-
Potentiation at the molecular layer interneuron–Purkinje cell synapse, which is facilitated by co-activition of the molecular layer interneuron and the climbing fibre innervating the same Purkinje cell.
- Harmaline
-
A tremorgenic drug that induces oscillations in neurons of the inferior olive.
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De Zeeuw, C., Hoebeek, F., Bosman, L. et al. Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci 12, 327–344 (2011). https://doi.org/10.1038/nrn3011
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DOI: https://doi.org/10.1038/nrn3011
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