Dexterity in cerebellar agenesis

Abstract

Given the well established role of the cerebellum in motor control, deficient motor performance during life time appears to be common in cerebellar agenesis. However, behavioural data on motor performance in living subjects with cerebellar agenesis are scarce. Dexterity during object manipulation was comparatively investigated in a 63-year old female with cerebellar agenesis and three healthy age- and gender-matched control subjects. Participants performed a transport task with an instrumented object and caught a weight that was dropped into a hand-held receptacle either expectedly from the opposite hand or unexpectedly from the experimenter's hand. Compared to healthy subjects, the subject with cerebellar agenesis generated greater grasping forces. For the transport task the patient showed a clear impairment of the predictive adjustment of grasping forces to the differential loading requirements of movement direction. For the weight-catching task, the patient established an accurate reactive mode of control when the weight was dropped unexpectedly. In case the weight was dropped expectedly from the opposite hand, predictive control mechanisms were severely disturbed in the subject with cerebellar agenesis. These data highlight the role of the cerebellum for predictive force control and are interpreted within the concept of internal models reflecting the causal relationship between actions and their consequences.

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.