The cerebellum for jocks and nerds alike
- Department of Neuroscience, University of Minnesota, Minneapolis, MN, USA
Historically the cerebellum has been implicated in the control of movement. However, the cerebellum’s role in non-motor functions, including cognitive and emotional processes, has also received increasing attention. Starting from the premise that the uniform architecture of the cerebellum underlies a common mode of information processing, this review examines recent electrophysiological findings on the motor signals encoded in the cerebellar cortex and then relates these signals to observations in the non-motor domain. Simple spike firing of individual Purkinje cells encodes performance errors, both predicting upcoming errors as well as providing feedback about those errors. Further, this dual temporal encoding of prediction and feedback involves a change in the sign of the simple spike modulation. Therefore, Purkinje cell simple spike firing both predicts and responds to feedback about a specific parameter, consistent with computing sensory prediction errors in which the predictions about the consequences of a motor command are compared with the feedback resulting from the motor command execution. These new findings are in contrast with the historical view that complex spikes encode errors. Evaluation of the kinematic coding in the simple spike discharge shows the same dual temporal encoding, suggesting this is a common mode of signal processing in the cerebellar cortex. Decoding analyses show the considerable accuracy of the predictions provided by Purkinje cells across a range of times. Further, individual Purkinje cells encode linearly and independently a multitude of signals, both kinematic and performance errors. Therefore, the cerebellar cortex’s capacity to make associations across different sensory, motor and non-motor signals is large. The results from studying how Purkinje cells encode movement signals suggest that the cerebellar cortex circuitry can support associative learning, sequencing, working memory, and forward internal models in non-motor domains.
The role of the cerebellum in the nervous system remains controversial. Traditionally, cerebellar function has been viewed in the context of motor control, given the well-established fact that cerebellar insults result in movement deficits. Different aspects of the cerebellum’s involvement in motor control have generated multiple hypotheses regarding cerebellar function including movement timing (Braitenberg and Atwood, 1958; Keele and Ivry, 1990; Welsh et al., 1995; O’Reilly et al., 2008), error detection and correction (Oscarsson, 1980), motor learning (Marr, 1969; Albus, 1971; Gilbert and Thach, 1977; Ito, 2002), and providing internal models (Wolpert et al., 1998; Kawato, 1999; Imamizu et al., 2000; Morton and Bastian, 2006; Shadmehr et al., 2010).
More recently, evidence for cerebellar involvement in non-motor processes such as cognition, emotions and social interaction has accumulated at a rapid pace. The findings include the rapid expansion of the cerebellar hemispheres in primates (Leiner et al., 1986, 1989) with development of projections between the cerebellum and non-motor cortical areas (Schmahmann and Pandya, 1989, 1991, 1997; Middleton and Strick, 1994, 2001; Kelly and Strick, 2003), cerebellar activation related to cognitive behaviors (Petersen et al., 1988; Kim et al., 1994; Hayter et al., 2007), cognitive and emotional dysfunction associated with cerebellar lesions/disease (Fiez et al., 1992; Schmahmann, 2004; Burk, 2007), and the influence on cognitive processes by manipulating cerebellar excitability (Ferrucci et al., 2008; Pope and Miall, 2012; Boehringer et al., 2013). These contributions to non-motor behaviors raise the question of whether the cerebellum performs specific computations/functions in different domains or performs a common process across all domains. Based on its stereotypical architecture, a plausible and parsimonious hypothesis is that the cerebellum performs a uniform process in both motor and non-motor processes (Schmahmann, 2000, 2010; Ramnani, 2006; Thach, 2007; Ito, 2008). An important implication of this hypothesis is that understanding cerebellar information processing in the motor domain can illuminate the contributions of the cerebellum in non-motor domains.
Working from the common processing viewpoint, this review argues that the present state of our understanding of the cerebellum’s role in motor behavior can shed light on non-motor functions. Several authors have taken a similar perspective (Ito, 2008; Imamizu and Kawato, 2009; Pezzulo, 2011; Pezzulo et al., 2012). An advantage of applying a motor control view to non-motor processing is that subjects, including non-human primates, can be required to perform extremely demanding motoric tasks in highly controlled environments. Despite task complexity, motor behavior can be described and quantified by well-defined measures, allowing intimate and unambiguous access to cerebellar signals. Therefore, this review evaluates the motor signals encoded by cerebellar neurons, including the existence of a new class of signals in Purkinje cell simple spike activity related to performance errors, as well as a dual encoding mechanism for motor parameters (Hewitt et al., 2011; Popa et al., 2012). Together, these signals could provide the neural substrate for computing sensory prediction errors postulated by internal model hypotheses (Wolpert and Ghahramani, 2000; Mazzoni and Krakauer, 2006; Shadmehr et al., 2010). We suggest these new findings regarding simple spike signaling in motor behaviors provide insights into cerebellar function that could help understanding cerebellar involvement in non-motor domains.