Cerebellar contribution to spatial event processing: characterization of procedural learning

Abstract

Recently, we demonstrated the prevalent role of cerebellar networks in the acquisition of the procedural components of spatial information by testing hemicerebellectomized (HCbed) rats in a classical spatial task, the Morris water maze (MWM). As procedures used in the water maze are a mixture of different components (that is, general procedures, exploration procedures, direct reaching procedures), for optimally solving a spatial task all procedural components must be opportunely managed. Thus, severely impaired procedural learning of cerebellar origin can be better comprehended by fractionating the procedural facets. To this aim, a two-step water-maze paradigm was employed. Normal rats were first trained to search for a hidden platform moved to a different position in each trial, utilizing a water maze setting in which visual cues were abolished by heavy black curtains surrounding the tank. In this paradigm, normal animals solved the task by using general and exploration procedures, but they could not use direct reaching skills. A subgroup of these pretrained animals was then HCbed and, after recovery from cerebellar lesion, was tested in a water maze with normal environmental cues available, a paradigm in which normal animals develop abilities for reaching the target with very direct trajectories. Pretrained HCbed animals, however, did not display the typical spatial deficits of naive HCbed rats, persisted in exhibiting the scanning strategy learned during pretraining, and never displayed direct reaching skills. In conclusion, cerebellar networks appear to be involved in the acquisition of all procedural facets necessary for shifting behavior within the maze until direct reaching of the platform. The lack of flexibility in changing exploration strategies displayed by pretrained HCbed rats is interpreted by taking into account the well-known cerebellar frontal interplay sculpting a specific cerebellar role in the acquisition of spatial procedural steps.

Representation of actions in rats: The role of cerebellum in learning spatial performances by observation

“…Because our previous findings demonstrated the prevalent role of cerebellar circuits in acquisition rather than in storage or recall of procedural exploration strategies (3,13,16), we specifically tested acquisition by observation in an experimental group in which the cerebellar lesion preceded observation training (HϩO group). When tested in the MWM, these rats completely lacked the learning effects of observation (Fig.…”

Changes in Cerebello-motor Connectivity during Procedural Learning by Actual Execution and Observation

“…Although most studies have shown that visuomotor procedural learning is related to changes in the synaptic efficacy of motor cortex, the hypothesis of a contribution of other cortical and subcortical structures to the learning-associated modulation of cortical excitability has not yet been investigated. In the last decade, the role of the cerebellum in the acquisition of procedural competencies has been widely demonstrated in studies on rats, healthy human subjects, and cerebellar patients (Torriero et al, 2004Leggio et al, 1999;Gòmez-Beldarrain et al, 1998;Petrosini, Molinari, & DellʼAnna, 1996). A recent magnetoencephalography study demonstrated that after a perceptual-motor task had been learned a decrease in motor cortical activity was accompanied by an increase in cerebellar activity (Houweling, Daffertshofer, van Dijk, & Beek, 2008).…”

“…Experimental findings show that the cerebellum is involved in learning new procedures during the actual execution of a task and during observational training (Ito, 2008;Petrosini, 2007;Torriero, Oliveri, Koch, Caltagirone, & Petrosini, 2004Leggio et al, 1999Leggio et al, , 2000 and, in particular, that it plays a key role in sequential procedural learning, as measured by a serial reaction time task (SRTT) (Gòmez-Beldarrain, Garcìa Moncò, Rubio, & Pascual-Leone, 1998;Molinari et al, 1997;Pascual-Leone, Grafman, Clark, Stewart, & Massaquoi, 1993). Furthermore, it has been shown that cerebellar rTMS decreases procedural learning during performance of an SRTT (Torriero et al, 2004) and interferes with acquisition of procedural competencies through observation .…”

The What and How of Observational Learning

“…Moreover, experimental findings demonstrate that in rats cerebellar lesions markedly impair the learning of new procedures not only by actual execution of a task (Leggio et al, 1999) but also by observation (Leggio et al, 2000). Thus, there are a number of indications that cerebellar circuits are involved in ''motor thought'' whether they are accompanied by actual motor acts.…”