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

Abstract

Experimental evidence demonstrates that cerebellar networks are involved in spatial learning, controlling the acquisition of exploration strategies without blocking motor execution of the task. Action learning by observation has been considered somehow related to motor physiology, because it provides a way of learning performances that is almost as effective as the actual execution of actions. Neuroimaging studies demonstrate that observation of movements performed by others, imagination of actions, and actual execution of motor performances share common neural substrates and that the cerebellum is among these shared areas. The present paper analyzes the effects of observation in learning a spatial task, focusing on the cerebellar role in learning a spatial ability through observation. We allowed normal rats to observe 200 Morris water maze trials performed by companion rats. After this observation training, ''observer'' rats underwent a hemicerebellectomy and then were tested in the Morris water maze. In spite of the cerebellar lesion, they displayed no spatial defects, exhibiting exploration abilities comparable to controls. When the cerebellar lesion preceded observation training, a complete lack of spatial observational learning was observed. Thus, as demonstrated already for the acquisition of spatial procedures through actual execution, cerebellar circuits appear to play a key role in the acquisition of spatial procedures also through observation. In conclusion, the present results provide strong support for a common neural basis in the observation of actions that are to be reproduced as well as in the actual production of the same actions. R ecent findings demonstrated that the cerebellum must be included in the neural substrates that process spatial information (1-4). Whereas neocortical and hippocampal regions are involved in memory for spatial and object information and in locating objects in a given environment (5-8), the cerebellum appears to be involved in the navigational system with overt procedural features that control the way to reach an object, explore a new environment, and acquire spatial knowledge in relation to personal orientation. Thus, the cerebellar function is specifically linked to ''how to find an object'' rather than ''where the object is'' (9). This evidence mainly results from experimental data reporting that in the Morris water maze (MWM), hemicerebellectomized (HCbed) rats are impaired in developing efficient exploration strategies, but not in locating platform position (3). When the task is proposed for the first time postoperatively, HCbed animals display only peripheral circling around the pool, a rather ineffective way of acquiring spatial information. Conversely, when spatial procedures are acquired by executing the MWM task preoperatively, the cerebellar lesion does not alter spatial task execution.Thus, these findings demonstrate that cerebellar circuitry is involved only (or primarily) in the acquisition of procedural components of spatial tasks and that a cerebellar le...

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

“…Experimental findings have also revealed the cerebellar role in the acquisi-tion of procedural competencies, even when learning is acquired by observation. Cerebellar lesions in rats induced deficits in spatial learning by observation; nevertheless, once acquired, spatial procedures were not impaired even in the presence of cerebellar damage Leggio et al, 2000). It was also found that although rTMS applied over the cerebellum interferes with observational learning of new procedures, cerebellar rTMS applied after observational training does not influence task execution .…”

“…An increasing number of experimental and neuroimaging findings point to cerebellar involvement in "motor thought" (Schmahmann, 2004). In rats, cerebellar lesions markedly impaired the learning of new procedures not only during the actual execution of a task (Mandolesi, Leggio, Spirito, Federico, & Petrosini, 2007;Mandolesi, Leggio, Spirito, & Petrosini, 2003;Mandolesi, Leggio, Graziano, Neri, & Petrosini, 2001;Petrosini et al, 1996) but also during observation (Leggio et al, 2000). Likewise, cerebellar activation has been reported during the observation of actions that have to be subsequently imitated (Frey & Gerry, 2006;Jackson, Meltzoff, & Decety, 2006;Leslie, Johnson-Frey, & Grafton, 2004;Chaminade, Meltzoff, & Decety, 2002;Decety et al, 1994).…”

“…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.…”

Neuropsychiatry of creativity

“…Evidence suggests that the cerebellum is involved in the link between seeing and doing -or processing movements and behaviour that have been observed, for the individual to produce them later [14]. The cerebellum is also critically involved in the internal representation of action, an ability used to understand and learn the skills of others by observation.…”