Dexterity in cerebellar agenesis
Introduction
Complete absence of the cerebellum is extremely rare with only a few cases reported in the literature since the first description in 1831 (Combettes, 1831, Priestley, 1920, Rubinstein and Freeman, 1940; Titomanlio, Romano, & Del Giudice, 2005; Velioglu, Kuzeyli, & Özmenoglu, 1998; for a review see Glickstein, 1994, Macchi and Bentivoglio, 1977). The majority of cases have been found post-mortem and the debate of whether or not motor performance is impaired in cerebellar agenesis is still unsettled. Given the well established role of the cerebellum in motor control and motor learning (Courchesne & Allan, 1997; Glickstein & Yeo, 1990; Middleton & Strick, 1997; Nowak et al., in press, Thach, 1998), deficient motor performance during life time appears to be common in cerebellar agenesis (see Glickstein, 1994 for a detailed review). However, behavioural data on motor performance in living subjects with cerebellar agenesis are hardly available (Richter et al., 2005, Timmann et al., 2003) and a detailed description of manual dexterity is still lacking in this entity.
The exquisite control of grasping forces when manipulating objects in the environment is an essential part of our daily motor repertoire. Skilled control of grasping forces involves different modes of control which rely on prediction and sensory feedback to different extents. When we handle objects in the environment that exhibit stable properties, predictive control mechanisms can effectively be exploited. When, for example, the load of a hand-held object is increased by a self generated action – such as moving the arm during a transport movement or dropping a weight from one hand into a receptacle held by the opposite hand – grasping forces increase in parallel with load forces without an obvious time delay (Flanagan & Wing, 1993; Johansson & Westling, 1988). When, on the other hand, we handle objects with unpredictable behaviour-like catching a weight that is unexpectedly dropped from another person into a hand-held receptacle – sensory feedback provides the most useful source to signal a change in load with the consequence that grasping forces tend to lag behind load (Johansson & Westling, 1988).
The predictive coupling between grasping and load force profiles has been interpreted within the theoretical concept of internal forward models (Wolpert & Flanagan, 2001). Given the regular anatomical cytoarchitecture of the cerebellar cortex and the well characterised functional circuitry with only one output cell and four main classes of interneurons, the cerebellum has been considered to incorporate such internal forward models (Wolpert, Miall, & Kawato, 1998). Indeed, single cell recordings obtained from cerebellar Purkinje cells and deep cerebellar nuclei suggest that cerebellar activity is closely linked to predictive mechanisms of grasping (Espinoza & Smith, 1990; Monzée & Smith, 2004). In addition, behavioural data have demonstrated that predictive control of grasping is severely impaired while reactive mechanisms of force control appear to be well preserved in subjects with cerebellar disorders (Babin-Ratté et al., 1999, Nowak et al., 2002, Nowak et al., 2004, Rost et al., 2005).
Here we report on the control of grasping forces in a case of cerebellar agenesis. Both predictive and reactive control mechanisms were tested. Based on behavioural data (Babin-Ratté et al., 1999, Nowak et al., 2002, Nowak et al., 2004, Nowak et al., 2005), single cell recordings (Espinoza & Smith, 1990; Monzée & Smith, 2004) and recent theoretical concepts on the role of the cerebellum for predictive motor control (Wolpert et al., 1998, Wolpert and Flanagan, 2001) we expected a clear deficit of predictive, but not reactive force control mechanisms in cerebellar agenesis.
Section snippets
Participants
A 63-year old right-handed white female (H.K.) with almost complete absence of the cerebellum as revealed by magnetic resonance imaging (Fig. 1) participated in the experiments. H.K.'s past medical and family histories have been described earlier in detail (Timmann et al., 2003). Neurological examination revealed mild to moderate cerebellar dysarthria, mild to moderate ataxia of the upper and lower limbs, mild ataxia of stance and impaired gait. Her gait disorder was aggravated by a marked
Results
The minimum grip forces necessary to prevent the object from slipping were similar for H.K. (2.6 ± 0.2 N) and the healthy control subjects (2.5 ± 0.2 N). Thus, any differences in the efficiency of grip force scaling between H.K. and the healthy control subjects could not be due to variations in the frictional condition at the skin-object interface.
Discussion
The present study was intended to investigate both predictive and reactive control mechanisms of dexterous manipulation in a case of cerebellar agenesis. Our data clearly demonstrate that the cerebellum appears to play a vital role for the predictive control of grasping, whereas it is less involved in reactive force control mechanisms. In the following we will discuss these findings in the context of recent theoretical concepts and lesion data, suggesting that the cerebellum is essential to
Conclusion
The efficiency and coordination of grasping forces during object manipulation was investigated in a case of cerebellar agenesis. Both predictive and reactive control mechanisms were tested. Compared to healthy control subjects, the subject with cerebellar agenesis produced excessive grasping forces and exhibited a clear deficit of predictive, but not of reactive force control mechanisms. These data highlight the role of the cerebellum for predictive motor performance and may be interpreted
Acknowledgement
The authors are indebted to H.K. and the healthy subjects for their willingness to participate in the current project. The project was supported by a grant of the Deutsche Forschungsgemeinschaft (DFG Ti-239/8-1 and He-3592/4-1).
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