During object manipulation tasks, the brain selects and implements action-phase controllers that use sensory predictions and afferent signals to tailor motor output to the physical properties of the objects involved. Analysis of signals in tactile afferent neurons and central processes in humans reveals how contact events are encoded and used to monitor and update task performance.

Coding and use of tactile signals from the fingertips in object manipulation tasks

The roles and functions of cutaneous mechanoreceptors.

The hypothesis that the central nervous system (CNS) generates movement as a shift of the limb's equilibrium posture has been corroborated experimentally in studies involving single- and multijoint motions. Posture may be controlled through the choice of muscle length-tension curve that set agonist-antagonist torque-angle curves determining an equilibrium position for the limb and the stiffness about the joints. Arm trajectories seem to be generated through a control signal defining a series of equilibrium postures. The equilibrium-point hypothesis drastically simplifies the requisite computations for multijoint movements and mechanical interactions with complex dynamic objects in the environment. Because the neuromuscular system is springlike, the instantaneous difference between the arm's actual position and the equilibrium position specified by the neural activity can generate the requisite torques, avoiding the complex "inverse dynamic" problem of computing the torques at the joints. The hypothesis provides a simple, unified description of posture and movement as well as contact control task performance, in which the limb must exert force stably and do work on objects in the environment. The latter is a surprisingly difficult problem, as robotic experience has shown. The prior evidence for the hypothesis came mainly from psychophysical and behavioral experiments. Our recent work has shown that microstimulation of the frog spinal cord's premotoneural network produces leg movements to various positions in the frog's motor space. The hypothesis can now be investigated in the neurophysiological machinery of the spinal cord.

Does the nervous system use equilibrium-point control to guide single and multiple joint movements?

The purpose of this study was to determine the precision of proprioceptive localization of the hand in humans. We derived spatial probability distributions which describe the precision of localization on the basis of three different sources of information: proprioceptive information about the left hand, proprioceptive information about the right hand, and visual information. In the experiment subjects were seated at a table and had to perform three different position-matching tasks. In each task, the position of a target and the position of an indicator were available in a different combination of two of these three sources of information. From the spatial distributions of indicated positions in these three conditions, we derived spatial probability distributions for proprioceptive localization of the two hands and for visual localization. For proprioception we found that localization in the radial direction with respect to the shoulder is more precise than localization in the azimuthal direction. The distributions for proprioceptive localization also suggest that hand positions closer to the shoulder are localized more precisely than positions further away. These patterns can be understood from the geometry of the arm. In addition, the variability in the indicated positions suggests that the shoulder and elbow angles are known to the central nervous system with a precision of 0.6-1.1 degrees. This is a considerably better precision than the values reported in studies on perception of these angles. This implies that joint angles, or quantities equivalent to them, are represented in the central nervous system more precisely than they are consciously perceived. For visual localization we found that localization in the azimuthal direction with respect to the cyclopean eye is more precise than localization in the radial direction. The precision of the perception of visual direction is of the order of 0.2-0.6 degrees.

The precision of proprioceptive position sense

This target article draws together two groups of experimental studies on the control of human movement through peripheral feedback and centrally generated signals of motor commands. First, during natural movement, feedback from muscle, joint, and cutaneous afferents changes; in human subjects these changes have reflex and kinesthetic consequences. Recent psychophysical and microneurographic evidence suggests that joint and even cutaneous afferents may have a proprioceptive role. Second, the role of centrally generated motor commands in the control of normal movements and movements following acute and chronic deafferentation is reviewed. There is increasing evidence that subjects can perceive their motor commands under various conditions, but that this is inadequate for normal movement; deficits in motor performance arise when the reliance on proprioceptive feedback is abolished either experimentally or because of pathology. During natural movement, the CNS appears to have access to functionally useful input from a range of peripheral receptors as well as from internally generated command signals. The unanswered questions that remain suggest a number of avenues for further research.

Does the nervous system depend on kinesthetic information to control natural limb movements

Spherically curved surfaces were applied, with controlled force, to the fingerpads of human subjects; their fingers were immobilized. The curvature of the surfaces was characterised by the reciprocal of the radius of curvature. In scaling experiments, the subjects' perceived magnitude of curvature increased markedly with an increase in the curvature of the stimulus. An increase in contact force resulted in a slight decrease in perceived curvature. Four discrimination experiments were performed using a forced choice paradigm. Subjects could discriminate, at the 75% level, a flat surface (zero curvature) from a convex curvature of 4.9 m-1 (radius of curvature 204 mm) and from a concave curvature of 5.4 m-1 (radius 185 mm). When discriminating 2 convex spherical surfaces, subjects could discriminate a curvature of 144 m-1 from a curvature of 158 m-1 (radii 6.95 and 6.33 mm reespectively), and could discriminate a curvature of 287 m-1 from one of 319 m-1 (radii 3.48 and 3.13 mm respectively); the Weber fraction is about 0.1. Contact areas between the curved surfaces and the fingerpad skin were estimated. There was approximate correspondence between contact areas and the scaling functions.

Tactile discrimination of curvature by humans using only cutaneous information from the fingerpads.

Human subjects scaled gratings of alternating grooves and ridges for perceived roughness. Roughness increased with an increase in groove width and decreased with an increase in ridge width, but the effect of groove width was much greater than the effect of ridge width. In corresponding neurophysiological experiments, the gratings were moved sinusoidally across the receptive fields of single mechano-receptive afferents innervating the fingerpads of anesthetized monkeys. The measure of response used was the mean cyclic discharge rate (averaged over one cycle of the sinusoid). Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) all showed a marked increase in response when groove width increased. An increase in ridge width had no consistent effect on the responses of SAs or RAs but resulted in a small decrease in the response of PCs. The response to a smooth surface differed significantly from the responses to the finer gratings only for the RAs. An alternative measure of response (the number of impulses elicited by each spatial cycle of the grating) increased with an increase in ridge width for all 3 fiber types. Thus, the large effect of groove width on perceived roughness can be accounted for by the mean cyclic discharge rate in the active afferent fibers. The smaller effect of ridge width can be accounted for by the number of impulses per spatial cycle of the grating.

https://www.jneurosci.org/content/jneuro/9/4/1273.full.pdf

Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad

The ability of human subjects to discriminate plane metal plates of different thickness was measured using a forced-choice paradigm. The plates, made by electroplating a thin layer of copper onto flat brass shims, were gripped between the thumb and the index finger. Subjects were presented with either 2 standard plates (0.2 mm thick), or a standard plate and a test plate that was slightly thicker, and were required to state which alternative had occurred. When the edges of the plates could not be touched, a difference in thickness of about 0.075 mm could be discriminated. Surprisingly, when the edges were included in the grip, performance did not improve. All hypotheses of strategies used by the subjects required them to sense the angles of the finger joints with a precision of about 0.1°.

Tactile discrimination of thickness.

Gratings of alternating grooves and ridges were moved sinusoidally across the fingerpads of anesthetized monkeys, while responses were recorded from individual slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) in the median nerve. The stimulus comprised 2 spatial variables, namely, groove width (G) and ridge width (W), and 2 temporal variables, namely, the peak speed of movement (S) and the peak temporal frequency (F) at which successive spatial cycles of the grating pass over a point in the receptive field. The responses of all 3 fiber types were determined by only 1 spatial variable, G, and only 1 temporal variable, F. Changes in W or S affected responses only if there was a concomitant change in either G or F. Responses were phase-locked to the occurrence of successive spatial cycles of the grating, and we have used the number of impulses elicited by a single spatial cycle as the fundamental measure of response. An equation of the form I = cGaexp(-b square root of F) describes the responses of all 3 fiber types. For SAs, the effect of groove width was greater (a = 2.64) than for RAs and PCs (a = 0.924 and 1.05, respectively). The reduction in response with frequency was most marked for SAs (b = 0.262), and greater for PCs (b = 0.167) than for RAs (b = 0.130). From the equation, the instantaneous response during the entire sinusoidal cycle was reconstructed as well as a second measure, the mean cyclic response. These 2 measures behaved differently with changes in the stimulus parameters. The temporal properties of the fibers, as revealed by gratings, may appear to be in conflict with those established by vibratory threshold studies; in fact, they are compatible with suprathreshold responses to vibrating probes.

https://www.jneurosci.org/content/jneuro/9/4/1280.full.pdf

Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad.

Skin on the fingertips of humans and monkeys was stimulated by a probe vibrating with a sinusoidal displacement. The probe and the skin were illuminated stroboscopically and were viewed through a dissecting microscope. The stroboscope was triggered by the sinusoidal generator via a digital delay, so that the position of both the probe and the skin could be measured at regular intervals during the cycle. Six frequencies and 3 amplitudes of vibration were used. During a portion of the cycle the probe and the skin separated, so that the skin waveform was a clipped sinusoid. An increase in stimulus frequency increased the fraction of the cycle during which the probe and the skin were separated. Adding a static pre-indentation to the vibration reduced this fraction, and for this condition a decrease in vibratory amplitude also decreased the fraction. Thus the skin motion contained harmonics that were not present in the probe motion, and the harmonic content differed for different stimulus conditions.

K. T. John

Papers

Tactile discrimination of curvature by humans using only cutaneous information from the fingerpads.

Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad

Tactile discrimination of thickness.

Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad.

Skin profiles during sinusoidal vibration of the fingerpad.