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  • Review Article
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Anatomical and physiological foundations of cerebellar information processing

Key Points

  • The cerebellum is crucial for the coordination of movement. Here, we present a model of the cerebellar paravermis, a region concerned with the control of voluntary limb movements through its interconnections with the spinal cord. We particularly focus on the olivo–cerebellar climbing fibre system.

  • Climbing fibres are proposed to convey motor error signals (signals that convey information about inappropriate movements) related to elementary limb movements that result from the contraction of single muscles. The actual encoding of motor error signals is suggested to depend on sensorimotor transformations carried out by spinal modules that mediate nociceptive withdrawal reflexes.

  • The termination of the climbing fibre system in the cerebellar cortex subdivides the paravermis into distinct microzones. Functionally similar but spatially separate microzones converge onto a common group of cerebellar nuclear neurons. The processing units formed as a consequence are termed 'multizonal microcomplexes' (MZMCs), and are each related to a specific spinal reflex module.

  • The distributed nature of microzones that belong to a given MZMC is proposed to enable similar climbing fibre inputs to integrate with mossy fibre inputs that arise from different sources. Anatomical results consistent with this notion have been obtained.

  • Within an individual MZMC, the skin receptive fields of climbing fibres, mossy fibres and cerebellar cortical inhibitory interneurons appear to be similar. This indicates that the inhibitory receptive fields of Purkinje cells within a particular MZMC result from the activation of inhibitory interneurons by local granule cells.

  • On the other hand, the parallel fibre-mediated excitatory receptive fields of the Purkinje cells in the same MZMC differ from all of the other receptive fields, but are similar to those of mossy fibres in another MZMC. This indicates that the excitatory input to Purkinje cells in a given MZMC originates in non-local granule cells and is mediated over some distance by parallel fibres.

  • The output from individual MZMCs often involves two or three segments of the ipsilateral limb, indicative of control of multi-joint muscle synergies. The distal-most muscle in this synergy seems to have a roughly antagonistic action to the muscle associated with the climbing fibre input to the MZMC.

  • Our model indicates that the cerebellar paravermis system could provide the control of both single- and multi-joint movements. Agonist–antagonist activity associated with single-joint movements might be controlled within a particular MZMC, whereas coordination across multiple joints might be governed by interactions between MZMCs, mediated by parallel fibres.

Abstract

A coordinated movement is easy to recognize, but we know little about how it is achieved. In search of the neural basis of coordination, we present a model of spinocerebellar interactions in which the structure–functional organizing principle is a division of the cerebellum into discrete microcomplexes. Each microcomplex is the recipient of a specific motor error signal — that is, a signal that conveys information about an inappropriate movement. These signals are encoded by spinal reflex circuits and conveyed to the cerebellar cortex through climbing fibre afferents. This organization reveals salient features of cerebellar information processing, but also highlights the importance of systems level analysis for a fuller understanding of the neural mechanisms that underlie behaviour.

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Figure 1: Basic structure of the cerebellar cortex.
Figure 2: Connectivity of the cerebellum.
Figure 3: Mapping of cerebellar cortical microzones.
Figure 4: Parallel processing in cerebellar microcomplexes.
Figure 5: Quantitative comparison of receptive fields.
Figure 6: Sensorimotor transformations in spinal nociceptive withdrawal reflex modules.
Figure 7: Postnatal developmental tuning of sensorimotor transformations in rat spinal nociceptive withdrawal reflex modules.
Figure 8: Receptive fields in the cerebellar cortex.
Figure 9: Input–output relationships.
Figure 10: Spinocerebellar interactions and motor coordination.

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Acknowledgements

The authors are grateful to J. Schouenborg for his comments on an earlier version of the manuscript. Many thanks are also due to R. Bissett for her help in the drafting of figures. We thank the UK Medical Research Council (R.A.) and the Swedish Research Council and the Segerfalk Foundation (M.G.) for their financial support.

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Glossary

PARAVERMIS

A region on either side of the midline of the cerebellum that lies lateral to the vermis and medial to the hemisphere. It contains the cerebellar cortical zones C1, C2 and C3 and receives climbing fibre input from the inferior olive and projects to the nucleus interpositus. Here, the term is used to denote the functionally related C1, C3 and Y (but not the C2) zones.

MOTOR ERROR

In the case of motor commands, the difference between the actual motor command and the correct command, or between the intended and achieved movement. A simple example is the retinal slip signal, in which this difference is detected directly at the sensory surface by specialized retinal ganglion cells.

GAIN

The amplification factor that regulates the relationship between input and output, for instance, in a reflex circuit.

TIMING THEORY

Here, the term refers to Braitenberg's idea that parallel fibres provide delay lines for converting spatial patterns into temporal patterns.

LEARNED PATTERN RECOGNITION THEORIES

Here, the term refers to the theories of Marr and Albus, in which the cerebellum is viewed as a spatial pattern recognition device with learning capacity.

CONTROL THEORY

Here, the term refers to a conceptual framework wherein engineering control principles are applied to the modelling of CNS functions.

ERROR-DETECTION HYPOTHESIS

The general idea that climbing fibres (detect and) convey signals that reflect errors in motor performance (posture as well as overt movement).

PARAFLOCCULUS

In experimental animals, the dorsal and ventral paraflocculus are the two most caudal lobules of the cerebellar hemisphere.

RETINAL SLIP

An unwanted movement of the visual image on the retina that occurs, for instance, when the movement of the eyes is inadequate to follow a moving object.

WITHDRAWAL EFFICACY

The motor effect of a muscle in terms of its movement away from an external reference point, which can be represented as a quantitative topographical map based on an analysis of the displacement of many points on the skin during the contraction of a single limb muscle.

IMPRINT

In the SNWR system there is, for each individual muscle, a close relationship between the distribution of sensitivity in the receptive field on the skin and the pattern of skin withdrawal caused by muscle contraction. Therefore, the output of the single muscle reflex component appears to be 'imprinted' on the spinal reflex circuitry that carries out the input–output transformation.

CEREBELLAR FEEDBACK-ERROR-LEARNING MODEL

A cerebellar model proposed by Kawato and colleagues that specifically addresses the issue of how sensory errors might be transformed into motor errors.

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Apps, R., Garwicz, M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6, 297–311 (2005). https://doi.org/10.1038/nrn1646

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