The evolution of manual dexterity

The unique capabilities of the human hand enable us to perform extremely fine movements, such as those needed to write or to thread a needle. The emergence of these capabilities was undoubtedly essential in human evolution: a combination of individually movable fingers, opposable thumbs and the ability to move the smallest finger and ring finger into the middle of the palm to meet the thumb gives us dexterity that is unparalleled in the animal kingdom.

Last year, geneticists identified a stretch of DNA which has undergone rapid change in humans but not in chimps, our closest relatives, or in other organisms. This short DNA sequence, named HACNS1, regulates the activity of genes involved in limb development. In chimps, it is active only in the upper arm, but in humans, it is active in the part of the hand which is destined to become the thumb, and so it was proposed to have been involved in the evolution of thumb opposability.

Neurobiologists from the University of Pittsburgh have now discovered a neuroanatomical specialization which also seems to have been important in the emergence of manual dexterity. In Proceedings of the National Academy of Sciences, they report that the area of the brain which controls voluntary movement in the higher primates is subdivided into two distinct regions, one of which is evolutionarily more recent and is essential for highly skilled movements.

Voluntary movements are controlled largely by the primary motor cortex (M1), which is located toward the back of the frontal lobe. The cells in this region of the brain have long axons which descend in a bundle of nerve fibres called the corticospinal tract and form connections with neurons in the spinal cord. M1 contains two general types of neurons: the axons of one type terminate in the intermediate layers of the cord, where they form synapses with interneurons which in turn synapse with the motor neurons, whose axons project out into the periphery to control the muscles. The other type send their axons further into the spinal cord, and connect directly to the motor neurons.

Jean-Alban Rathelot and Peter Strick injected rabies virus into single shoulder, elbow and finger muscles of rhesus monkeys (Macaca mulatta), so that the viral particles are transferred from the muscles to the nerve terminals of the motor neurons innervating them. Once there, the particles move along the axon toward the cell body in the spinal cord. (This process is called retrograde transport; retrograde means backwards, and refers to the movement of the virus in relation to the direction in which nervous impulses are propagated). Upon reaching the cell body, the virus traverses the synapse and then enters the cell or cells which form connections with the motor neuron. 

This technique, which is called retrograde tracing, therefore enabled the researchers to identify those spinal motor neurons which form direct connections with the axons descending from area M1, and those which form indirect connections via the interneurons. It revealed a surprising pattern: the vast majority of M1 neurons which connect directly to spinal motor neurons were found in a discrete region of the primary motor cortex, buried within the anterior (front) bank of the central sulcus, the prominent fissure which separates M1 from the primary somatosensory cortex. By contrast, the M1 neurons which form synapses with spinal interneurons were located in another immediately adjacent discrete subdivision, lying on the external surface of the frontal lobes. This is the first time that such a subdivision has been observed in area M1.

Earlier comparative anatomical had shown that direct but weak cortical-to-motor neuron connections are present in Old and New World monkeys, and that these descending pathways are far more prominent in the great apes and in humans. The functional consequences of these differences are nicely illustrated by comparing capuchin and squirrel monkeys, which, in terms of biomechanics, have very similar hands. However, capuchins have prominent direct inputs from the motor cortex onto motor neurons in the spinal cord; they can therefore move their fingers independently of each other to pick up small objects and manipulate tools. By contrast, squirrel monkeys have a weak direct input to spinal motor neurons, and as a result can only pick up small objects by sweeping movements of the hand in which all the fingers act together.     

Hence, the M1 subdivision containing neurons which synapse directly with spinal motor neurons is an evolutionarily newer structure, which is apparently unique to the higher primates, and was "added" during the course of evolution. The region containing cells which form indirect connections with motor neurons via the interneurons is phylogenetically older and is a common feature in many other mammalian species. This is recapitulated in development: in macaques, the indirect connections are present at birth, but the direct connections form postnatally. This probably accounts for the slow and gradual development of fine motor skills in human infants. The direct connections can override the intrinsic spinal cord circuitry, allowing for the generation of more flexible and complex patterns of muscular activity. The emergence of the "new" M1 region during evolution of the primate lineage is therefore likely to have been important for the enhanced manual dexterity of the human hand.

Related:

• Rabid brain circuits
• The baller's brain (and his pinky)
  
• Wilder Penfield, Neural Cartographer
  

Rathelot, J.-A. & Strick, P. L. (2009). Subdivisions of primary motor cortex based on cortico-motoneuronal cells Proc. Nat. Acad. Sci. DOI: 10.1073/pnas.0808362106