How predictive is grip force control in the complete absence of somatosensory feedback?

DOI: 10.1093/brain/awh016 Advanced Access publication October 21, 2003 Brain (2004), 127, 182±192 How predictive is grip force control in the complete absence of somatosensory feedback? Dennis A. Nowak,1 Stefan Glasauer3 and Joachim HermsdoÈrfer2 of Neurology and Clinical Neurophysiology, and 2Neuropsychology Research Group (EKN), Academic Hospital Bogenhausen, Technical University of Munich and 3Department of Neurology, Klinikum Groûhadern, Ludwig-Maximilians-University of Munich, Germany Summary Grip force control relies on accurate internal models of the dynamics of our motor system and the external objects we manipulate. Internal models are not ®xed entities, but rather are trained and updated by sensory experience. Sensory feedback signals relevant object properties and mechanical events, e.g. at the skin±object interface, to modify motor commands and update internal representations automatically. Here we prove that intact sensory feedback is essential for predictive grip force regulation. The ef®ciency and precision of grip force adjustments to load ¯uctuations arising from vertical and horizontal point-to-point arm movements with a hand-held object were analysed in a chronically deafferented subject (G.L.) and three healthy control subjects. Point-to-point movements started and ended with the object being held stationary. G.L. and healthy Correspondence to: Dr Dennis A. Nowak, Department of Neurology and Clinical Neurophysiology, Academic Hospital MuÈnchen Bogenhausen, Technical University of Munich, Englschalkingerstrasse 77, D-81925 Munich, Germany E-mail: controls produced similar accelerations of the grasped object and consequently similar load magnitudes during vertical and horizontal movements. Compared with healthy controls, G.L. employed inef®ciently high grip forces when holding and moving the object, indicating inaccurate force scaling to object weight and inertial loads. For healthy controls, the grip force pro®le was precisely timed to the movement-induced load ¯uctuations during vertical and horizontal movements. However, G.L.'s grip force pro®le was not processed to match differential loading requirements of movement direction. We conclude that predictive grip force control requires at least intermittent sensory feedback to signal the effectiveness of descending motor commands and to update internal models. Keywords: grip force; internal model; sensory feedback; proprioception; deafferentation Abbreviations: ACC = kinematic acceleration; GF = grip force; LF = load force Introduction Various environmental loads have to be counteracted in order to manipulate a hand-held object and prevent it from slipping when the external loads exceed the frictional force generated by gripping. When an object is held stationary in space, grip forces are adjusted according to the object's weight and surface friction (Johansson and Westling, 1984, 1991; Westling and Johansson, 1984a,b; Cadoret and Smith, 1996). Rapid and automatic grip force reactions compensate for unexpected load changes during restraint of a hand-held object (Johansson et al., 1992a,b,c). Grip force adjustments anticipate not only environmental demands, such as object weight and surface friction, but also the consequences of our own actions (Flanagan and Wing, 1993; Flanagan et al., 1995). When arm movements are used to transport a hand-held object, accelerations and decelerations induce inertial load ¯uctuations. In vertical point-topoint movements, clear grip force maxima occur at the time of maximum load peaks early in upward and late in downward movements (Flanagan et al., 1995; Flanagan and Wing, 1993; Flanagan and Tresilian, 1994). In horizontal point-to-point movements, two load force peaks occur during the acceleratory and deceleratory phases of the movement, regardless of movement direction. Here, grip force increases at the movement onset and remains elevated over the entire movement course, exhibiting one or two force peaks that coincide with one or both load force peaks. Thus, the timing of peak grip force depends on the timing of peak load force. The absence of a temporal delay between grip and load force Brain Vol. 127 No. 1 ã Guarantors of Brain 2003; all rights reserved 1Department Grip force control in a deafferented woman Somatosensory feedback provides the relevant information to acquire, maintain and update internal representations related to the dynamics of our own body and the relevant object properties. We hypothesized that if somatosensory feedback establishes internal representations, then deafferented subjects, without cutaneous and proprioceptive input, may contribute to our understanding of the relationships between anticipatory and feedback mechanisms during grip force control. We investigated grip force control in a deafferented subject, who performed vertical and horizontal point-to-point movements with a hand-held object. G.L. has had no tactile or proprioceptive sensations below the V2 cranial nerve division for over two decades now (Forget and Lamarre, 1987; Fleury et al., 1995; Simoneau et al., 1999). Consequently, she would not have been able to update her internal models about external object properties and the consequences of their manipulation on the basis of somatosensory input. We hypothesized that long-term deprivation of somatosensory feedback results in prediction errors during grip force control. G.L. lacks somatosensory information about the load magnitudes arising from object manipulation; this may result in reduced ef®ciency of her grip force scaling. In addition, sensory feedback may be essential to capture the timing of dynamic load ¯uctuations when moving a handheld mass and, consequently, the close temporal coupling between grip force and load force pro®les may be disrupted. Methods Subjects A 54-year-old deafferented subject (G.L.) and three healthy control subjects (control 1, female, 54 years old; control 2, male, 40 years old; control 3, male, 45 years old) participated. All subjects were right-handed and naive as to the purpose of the experiments. The deafferented patient suffered a permanent and speci®c loss of the large sensory myelinated ®bres in all four limbs following two episodes of sensory polyneuropathy that affected her whole body below the V2 cranial nerve division. The illness resulted in a complete loss of the senses of touch, vibration and pressure, and kinaesthesia in the neck, trunk, and upper and lower limbs, but temperature and pain sensation were preserved (Forget and Lamarre, 1987; Fleury et al., 1995; Simoneau et al., 1999). G.L. has no sensation or control of the head, neck or limb position and motion with eyes closed. These clinical observations were documented to be stable over the past two decades [a detailed clinical description of G.L. has been provided by Forget and Lamarre (1987)]. All subjects gave informed consent to participate in the study which was approved by the Ethics Committee of the (...truncated)