Constraints for control of the human hand

Abstract

More than 30 muscles drive the hand to perform a multitude of essential dextrous tasks. Here we consider new views on the evolution of hand structure and on peripheral and central constraints for independent control of the digits of the hand. The human hand is widely assumed to have evolved from hands like those of African apes, yet recent studies have shown that our hands and those of the earliest hominids are very similar and unlike those of living apes. Understanding the limits of hand function may come from investigation of our last common ancestor with the great apes, rather than the great apes themselves. In the periphery, movement across the full range of joint space can be limited by mechanical linkages among the extrinsic muscles. Further, peripheral limits occur when the hand adopts some positions in which the contraction of muscles fails to move the joints on which they usually act; there is muscle 'disengagement' and functional paralysis for some actions. Surprisingly, the central nervous system drives the hand seamlessly through this landscape of mechanical limits. Central constraints on control of the individual digits include the spillover of neural drive to neighbouring muscles and their 'compartments', and the inability to make maximal muscle forces when multiple digits contract strongly which produces a force deficit. The pattern of these latter constraints correlates with amounts of daily use of each digit and favours enslaved extension to lift fingers from an object but selective flexion of fingers to contact it.

Figure 1. Summary of possible links in schematic form

The distribution of output to individual muscles is intermingled at the level of the primary motor cortex and probably also at other supraspinal sites (1). Links can also occur at the level of the spinal cord, with some motoneurone pools receiving divergent inputs from corticofugal axons (2). Three major forearm muscles consist of multiple muscle bellies with tendons to each finger so that the muscles have four ‘compartments’ (3); there can be transfer of force between and within the different compartments of one muscle, but also between muscles (i.e. inter- and intramuscular force transfer). Furthermore, there are connections between the tendons for muscles on both the dorsal and ventral side of the hand (4).

Figure 2. Photographs of the hand to illustrate limits which occur in particular postures

A, when the hand is comfortably positioned with the fingers extended except that (say) the middle one is flexed, it is impossible to flex or extend its distal interphalangeal joint. It is functionally paralysed.B, when the other fingers are partially flexed, flexion but not extension is possible at the distal interphalangeal joint.C, the two hands are positioned with the middle phalanx of the index finger touching. In this position, the extensors of the index are functionally paralysed.D, grasping a test cylinder. This object can be instrumented to measure the forces under the pads of the digits. Note that the thumb must oppose the forces generated by the four fingers.

Figure 3. Data from a single subject to show the forces produced by single motor units in the flexor digitorum profundus on the finger pads during a weak static grasp of an instrumented cylinder

Each column represents data from a single unit. The spike-triggered average change in force under each finger produced by that unit is shown. The change in force under the test finger (red traces) was consistently greater than under the non-test fingers. However, both the ring-finger and little-finger motor units also produced relatively large forces under the adjacent finger (i.e. the little and ring fingers, respectively). (Modified from Kilbreath et al. 2002.)

Figure 4. Comparison of motor unit recruitment of the long multi-tendoned flexors and extensor of the human hand

A, the percentage of motor units that were not recruited at 50% of the maximal force (MVC) of the contracting digit for flexor digitorum profundus (FDP, open circles), flexor digitorum superficialis (FDS, filled circles), and extensor digitorum (ED, grey squares), depending on the distance between the test finger and the contracting digit.B, the percentage of motor units that were recruited below 10% MVC of the contracting digit for FDP (open circles) and ED (grey squares; unfortunately, these data are missing for FDS).C, the mean motor unit recruitment thresholds during voluntary contractions of non-test fingers are plotted for all index, middle, ring and little finger units of the FDS (filled circles), FDP (open circles) and ED (grey squares). (For original sources for panelCand further details see van Duinen et al. 2009.)

Figure 5. Force enslavement (red) and force deficits (blue) in flexion (left) and extension (right)

These two panels show both enslavement forces (in red) and force deficits (in blue) for all digits (T thumb; I index; M middle; R ring; L little finger) in single- and multi-digit tasks. A single-digit task is a task in which a subject is instructed to contract only one digit; however, the other digits show involuntarily produced force. In multi-digit tasks, two, three, four or five digits are instructed to move. In the five-digit tasks there is no enslavement. The enslaved force per digit is the average force produced by that digit when it was not a task digit. The ‘x’ for the little finger is the enslaved force for this finger when force produced in the opposite direction is not taken into account (so not part of a five-digit task). The force deficits (blue) are show on a scale from 100 down to 0% MVC. In this way low force deficits can be seen as high forces (higher lines in the figure). The force deficit in the different tasks for the separate digits is 100% MVC minus the average force of each digit when it is instructed to produce 100% MVC. Note the relatively low force deficits for the thumb in flexion and the relatively high force deficits of the thumb in extension. (Modified from Yu et al. 2010.)

Figure 6. The relation between individually daily use and force enslavement

This represents the percentage of individual daily use of the five digits (data from Ingram et al. 2008). The thumb is the digit used most frequently on its own, followed by the index finger. Daily use is plotted against the amount of enslavement in flexion (filled diamonds) and extension (open diamonds) of the individual digits in the single-digit tasks (data from Yu et al. 2010).