Tangential torque tunes touch

New insights into the role of tactile mechanoreceptors in the hand during object rotation are provided by Birznieks and colleagues (2010), in this issue of The Journal of Physiology, in an elegant study of the spike trains evoked by torsional and contact loads applied to the fingertips. The fine manipulative capacity provided by our fingers is possible because of their high sensory innervation density; if we lose tactile sensation in our fingers we lose manual dexterity. When we grasp an object in the hand and manipulate it, both predictive and sensory-guided mechanisms are engaged. Predictive feed-forward processes concerning the preferred grasp points and the initial applied grip force are normally employed at the outset of grasp (reviewed in Johansson, 1996; Wolpert & Miall, 1996; Flanagan & Wing, 1997). Somatosensory feedback from tactile receptors in the hand serves to confirm or refute these predictions, and to update learned grasp and manipulatory behaviours.

The grip and load forces used to lift an object are typically scaled by a small safety margin to maintain grasp stability while protecting the hand and object from damage (reviewed in Johansson, 1996; Johansson & Flanagan, 2009). These signals also serve to initiate corrective actions if errors occur, such as slippage of the object from the hand due to inadequate grip force. Most of these studies employed vertical lift in which tangential forces applied by gravity are in the plane of motion. However, when the grasp sites do not pass through the object's centre of mass, it tilts when lifted, adding tangential torque to the gravitational load force. Subjects compensate by applying additional grip force to prevent slippage (Kinoshita et al. 1997; Goodwin et al. 1998). Likewise, active rotation or tilt of objects held in the hand also generates tangential torques. For example, when we pour liquids from a bottle, we need to control both the flow rate and volume of liquid dispensed by altering wrist rotation and the relative forces applied by the thumb and other fingers.

Although tangential torques sensed by the fingertips form an important component of object manipulation, the effect of torque on the firing patterns of touch receptors has not been analysed. In this new report, Birznieks and colleagues (2010) applied torsional loads of two different magnitudes to the fingertips of anaesthetized monkeys using a pair of torque motors. They also measured the interaction between tangential torque and contact force by superimposing each torsional load on three different levels of normal forces. Birznieks et al. demonstrate that fast-adapting (FA-I) fibres from Meissner's corpuscles and slowly adapting (SA-I) fibres from Merkel cells play complementary roles in sensing tangential torque, and provide the necessary information to higher centres in the brain for controlling fingertip forces.

Both FA-I and SA-I afferents respond to changes in the magnitude and direction of tangential torque, but differ in the relative importance of specific stimulus features. FA-I fibres discriminate the onset and magnitude of changes in torque more accurately and rapidly than SA-I fibres, but rarely distinguish clockwise from anticlockwise rotations, or signal steady-state torques. FA-I fibres are silent during static grasp or lift actions when normal forces are constant. In contrast, SA-I fibres distinguish the applied normal force with latencies as brief as 250 ms, and also discriminate torque direction more accurately and faster than FA-I fibres. These findings suggest that FA-I fibres provide early warning signals of rotational as well as translational slips when objects held in the hand are manipulated or perturbed by external forces. The absence of tonic activity in FA-I fibres during static grasp enhances the sudden appearance of spike trains signalling object motion, aiding rapid adjustment of grip force in parallel with the onset of tangential motion over the skin (Kinoshita et al. 1997; Goodwin et al. 1998).

Interestingly, both SA-I and FA-I fibres were found to be more sensitive to torques if their receptive field centres were located adjacent to the area of direct skin contact with the object surface, suggesting that torsional forces and the accompanying microslips were greater away from the centre of rotation. These findings suggest that mechanoreceptors in the centre of the contact zone are particularly sensitive to normal forces, whereas tangential torque is more effective when stimulating the surrounding tissue. In this manner, important components of tactile stimuli are distributed in parallel across different receptor classes and neighbouring spatial domains on the skin.

In future studies it would be illuminating to investigate the combined effects of form, friction and torque on mechanoreceptor activity. Would the same results be obtained using curved (convex) contactors, or would changes in the skin contact area alter the sensitivity to torque as well as grip force? Would the simultaneous need to encode object shape enhance or interfere with the neural representation of torque parameters? The careful analyses and well-crafted experimental design presented by Birznieks et al. (2010) and earlier kinematic studies of torque by Goodwin et al. (1998) could serve as useful models for such studies.