Organizational Principles of Cerebellar Neuronal Circuitry

We review our recent studies of cerebellar neuronal organization, emphasizing that consideration of organizational features of cerebellar circuitry represents a necessary step toward the understanding of how the cerebellum does what it does, in terms of both its internal information processing and its interaction with other motor structures.

Whereas a variety of nonmotor cerebellar functions has been highlighted only recently, the role of the cerebellum in motor control has been acknowledged ever since the classical investigations carried out by Gordon Holmes, who demonstrated a number of characteristic abnormalities of movement in individuals suffering from cerebellar lesions due to gunshot injuries in the First World War. However, despite a long-standing general consensus regarding what the cerebellum does in motor control, at least in terms like “coordination of motor patterns,” the understanding of how it does what it does is still rather rudimentary (see Ref. 2 for a comprehensive exposé of the many controversies surrounding this topic).

Although recent use of brain imaging techniques in humans has shed some light on cerebellar involvement in the regulation of movement, the most direct way of addressing the issue of neuronal circuitry operation is by recording the unitary activity of cerebellar neurons in a behaving animal. In such paradigms, discharges of action potentials are analyzed in relation to the motor task under study, and correlations are sought between neuronal activity and different features of the movement performed, such as active force, limb displacement, preparation to move, or temporal and spatial characteristics of muscle activation. Typically, the neurons recorded during behavioral studies are described exclusively in terms of their discharge patterns, but little or no information is provided regarding other characteristics, such as their connectivity or peripheral receptive fields.

However, because synaptic connections are important for determining causes and consequences of neuronal activity, both the connectivity and the activity of the same neurons must be known to understand in detail how a central nervous structure fulfills its functions. A lack of assessment of overall attributes of cerebellar neurons recorded during behavioral studies precludes a full systematization of data and is therefore likely to hamper the progress of unraveling the mode of operation of cerebellar control systems. Given the specific connectivity of the cerebellar neuronal network and the complexity of its afferent input and efferent connections, any interpretation of how information is being processed from the input to the output, even in a given motor task, is bound to meet with difficulties when based on data collected from functionally heterogeneous populations of cells. Furthermore, because most cerebellar neuronal discharge patterns described do not seem to closely encode either the activity of single muscles or simple movement parameters, comparison between data collected in different studies using different motor tasks is difficult in the absence of a task-independent frame of reference for characterization of neurons.

With the above considerations in mind, in this report we draw attention to some aspects of the detailed functional connectivity of cerebellar neuronal circuitry. We suggest that emerging organizational principles of the cerebellum may provide a useful framework for characterization of neurons also in behavioral investigations and may aid in elucidating what type of afferent information reaches the cerebellar cortex, how this information is processed, and what the cerebellar output actually does.