The Roles of the Olivocerebellar Pathway in Motor Learning and Motor Control. A Consensus Paper

Abstract

For many decades the predominant view in the cerebellar field has been that the olivocerebellar system's primary function is to induce plasticity in the cerebellar cortex, specifically, at the parallel fiber-Purkinje cell synapse. However, it has also long been proposed that the olivocerebellar system participates directly in motor control by helping to shape ongoing motor commands being issued by the cerebellum. Evidence consistent with both hypotheses exists; however, they are often investigated as mutually exclusive alternatives. In contrast, here we take the perspective that the olivocerebellar system can contribute to both the motor learning and motor control functions of the cerebellum, and might also play a role in development. We then consider the potential problems and benefits of its having multiple functions. Moreover, we discuss how its distinctive characteristics (e.g., low firing rates, synchronization, variable complex spike waveform) make it more or less suitable for one or the other of these functions, and why its having a dual role makes sense from an evolutionary perspective. We did not attempt to reach a consensus on the specific role(s) the olivocerebellar system plays in different types of movements, as that will ultimately be determined experimentally; however, collectively, the various contributions highlight the flexibility of the olivocerebellar system, and thereby suggest it has the potential to act in both the motor learning and motor control functions of the cerebellum.

Inferior Olivary TMEM16B Mediates Cerebellar Motor Learning

“…The correlation between reduced IO excitability and impaired cerebellar motor learning in TMEM16B KO mice adds new evidence to support the theory that IO excitability and the subsequent climbing fiber impulses play a key role on the formation of cerebellar motor learning (Lang et al, 2017; Najafi and Medina, 2013). The prevailing view of cerebellar motor learning is that IO neurons relay movement error signals through climbing fiber spikes to cause synaptic modification in the cerebellar cortex, such as long-term depression (LTD) of parallel fiber to Purkinje cell synapses (Lang et al, 2017).…”

“…The prevailing view of cerebellar motor learning is that IO neurons relay movement error signals through climbing fiber spikes to cause synaptic modification in the cerebellar cortex, such as long-term depression (LTD) of parallel fiber to Purkinje cell synapses (Lang et al, 2017). Recent studies have clearly shown that, during motor learning, the number of climbing fiber spikes and the duration of the bursts, which reflect IO excitable state, control the number of spikelets within a complex spike waveform and the duration of the complex spike responses in Purkinje cells (Coesmans et al, 2004; Mathy et al, 2009; Rasmussen et al, 2013; Yang and Lisberger, 2014).…”

The Cerebellum: Adaptive Prediction for Movement and Cognition

“…Hence, the Purkinje cell simple spike activity could be viewed as constituting the sensory prediction [45, 46, 63] (although it may also contribute to the motor command), while the climbing fiber activity resulting in Purkinje cell complex spikes provides a representation of sensory prediction errors [64–66], driving cerebellar learning. It should be noted that, although this model has been highly influential in theories of cerebellar-based learning, there remains considerable debate over the functional role of the climbing fiber signals and their interaction with simple spike activity [50, 64, 67]. Furthermore, recent physiological data in mice and rats suggest cerebellar modules vary in the firing rate of simple spike activity and exhibit plasticity tuned to different time intervals between parallel and climbing fiber inputs [20, 21, 68].…”

In vivo analysis of synaptic activity in cerebellar nuclei neurons unravels the efficacy of excitatory inputs

“…Last, APs in CN neurons are generated by excitatory inputs. This was mentioned by Llinás & Mühlethaler (1988), further discussed by Gauck & Jaeger (2003) and summarized recently in Lang et al (2017).…”

“…This was mentioned by Llinás & Mühlethaler (), further discussed by Gauck & Jaeger () and summarized recently in Lang et al . ().…”