From the Archives
The intraneural topography of the radial, median and ulnar nerves. By Sydney Sunderland. Department of Anatomy and Histology, University of Melbourne. Brain 1945: 68; 245–99.Of the 18 papers appearing in Volume 68 of Brain, four are by Sydney Sunderland: he writes on ‘Arterial relations of the internal auditory meatus’, ‘Traumatic injuries of peripheral nerves’, ‘The adipose tissue of peripheral nerves’ and (here) ‘The intraneural topography of the radial, median and ulnar nerves’. Sunderland was Professor of Anatomy in the University of Melbourne; he was 35 when he wrote this paper in 1945, and had already held this post for 8 years. The question at issue for Sunderland was whether or not peripheral nerve contains discrete aggregations of nerve fibres wrapped (like a cable) in a connective tissue band, or an intraneural pattern resulting from repeated exchanges between funiculi producing ‘a plexiform arrangement of such bewildering complexity as to exclude the possibility of groups of fibres being confined throughout their course to a particular bundle or quadrant of the nerve’. His aim was to resolve, for the median, ulnar and radial nerves, the distance over which afferent and efferent fibres retain topography within the nerve trunk, or are subject to redistribution by division and anastomosis; whether such rearrangements create or disperse groups of fibres subserving related functions; and whether redistribution is selective, in either a coherent or a random fashion. Sunderland found the existing literature ambiguous on these points. He relied much on papers by J. Sherren (‘Injuries of nerves and their treatment’, 1907), J. N. Langley and M. Hashimoto (J Physiol 1917; 51: 318–46), W. M. Kraus and S. D. Ingham (Arch Neurol Psychiatr 1920; 4: 259–296) and J. C. McKinley (Arch Neurol Psychiatr 1921; 6: 377–399). Anatomical and histological considerations had initially led to the conclusion that peripheral nerve does have a cable structure, but this was later qualified by evidence for the plexiform nature of intraneural funicular patterns: but ‘it is not unlikely that some fibres keep their ... position in passing through the plexus since a complete crossing ... seems meaningless’. The initial studies of muscle contraction following electrical stimulation of separate nerve quadrants led to the conclusion that ‘the course is a straight one from the point where the nerve has been made up by its contributing segments to the point of offset of the fasciculi as a branch’. In noting that stimulation of the seven bundles of the peroneal nerve at the feline knee resulted in separate and predictable muscle responses, whereas electrical responses from the canine sciatic nerve at the ischium led all the muscles of the lower leg to contract—and taking into account the evidence that one-third of a proximal human nerve trunk could be sectioned without demonstrable effect—Sunderland began to see a way forward. Due to the intraneural topography and rearrangements, much must depend on the level of the damage and which axial component is lesioned or stimulated. This hypothesis also allowed him to explain why fibres undergoing Wallerian degeneration after high nerve section are widely distributed at distal levels: ‘it simply had not occurred to the investigators that the funicular organisation might be more marked distally than in the proximal nerve trunk’.
Sunderland dissected one median nerve, one radial nerve and two ulnar nerves, and all the branches, in their entirety and made 25 µm sections from bottom to top, staining the paraffin-embedded preparations with haematoxylin and eosin. Every tenth preparation was used to recreate the original funicular anatomy with special reference to the major branches, throughout the course of these nerves. The other sections were retained for reference. In the radial nerve, funiculi were strictly organized over the distal 7 cm, with some communications within but not between bundles. Moving proximally, the degree of fibre dispersal increased, locally at first and then starting to spread between bundles. Whereas the nerves to individual muscles could reliably be identified in discrete quadrants distally, the more proximal arrangement was for admixture. Thus, it was possible to strip individual nerves distally but not in the proximal nerve trunk. Whilst apparently less consistently organized, the median nerve also retained funicular integrity over its distal 5 cm but, as the nerve ascended, the scattering and intermingling of terminal branch fibres gradually eroded that localization; this applied both to the main nerve and to the nerve sections adjacent to each branch. Again, the ulnar nerve was organized into discrete bundles in its distal 9 cm, with some constraints discernible for a further 16 cm. Thereafter, funicular organization degenerated.
Sunderland was not confused about the definitive nature of his work. All ambiguities in the existing literature were reconciled by his demonstration that funicular organization altered across the proximal and distal segments of the three main nerves of the upper limb. Therefore it was no surprise that McKinley (1921) should have obtained a diffuse electrical reaction on stimulating the proximal nerve trunk, whereas Langley and Hashimoto (1917) stimulated distally and obtained organized responses. Variation in the level of injury was also the explanation for the clinical observations on partial nerve injury by James Sherren (1907). Explained thus, the proximal scatter of fibres within nerve trunks represented nothing more than the continuing reorganizations of segmental nerve root innervations taking place higher up in the brachial and lumbosacral plexuses, fibres for a particular branch being gradually gathered together as they approached their terminal distributions. But to Sunderland this was too simple, although he could not explain why the extent of sorting was far in excess of that needed to gather together cognate nerve fibres, why the components of certain branches continued to anastomose distally to the site of branching, and why some funiculi anastomosed and travelled as one before again dividing more distally.
Sunderland's main interest lay in the implications of this anatomy for understanding and improving the potential for recovery from peripheral nerve injury. ‘The effect of partial nerve section depends on the level of injury and the particular segment injured. ... partial proximal injury may involve ... only a few of the fibres of some, or all, branches so that the resultant loss of function cannot be detected clinically’. The chances reduce that injury will involve all or the majority of fibres for a particular branch, and hence produce clinical manifestations, as the nerve is ascended. Although he agreed with the observation of Seddon, Medawar and Smith (J Physiol 1943; 102: 191–215) that regeneration was less predictable when injury occurred close to a branch, and therefore involved a crucial collection of fibres rather than a scattered selection, not all of which were destined for that muscle, Sunderland did not share their interpretation that this related exclusively to the intraneural topography of funiculi and plexuses close to branches. His felt that too much rearrangement occurred at multiple proximal levels to allow such a strictly topographical analysis of nerve regeneration: ‘consequently there can be no distinction between lesions situated above and below the level of the plexus. ... a lesion that is not of uniform severity across the nerve even if situated at a considerable distance above the site of branching could result in obstruction of all the fibres destined for a branch. ... lesions well above the origin of branches may also have the same effect’. But for peripheral nerve surgeons, the need to respect axial organization when re-suturing peripheral nerve injuries, keeping the quadrants in continuity, was important—especially for distal injuries. It also followed that a greater length of distal than proximal nerve resection could be tolerated without losing funicular patterns, although the gradual rotations and twistings of these bundles in the intact nerve had to be respected by the restorative peripheral nerve surgeon. These torsions had been shown to be most prominent for the median nerve (at the wrist), intermediate for the ulnar, and least of a problem for the radial nerve. Perhaps this explained why reconstruction of the radial nerve offered the best clinical results.
In 1945, the anatomy of peripheral nerve injuries and nerve repair were matters of considerable social importance. Sunderland was responsible for a peripheral nerve injuries unit at the 115th Army General Hospital, Heidelberg, Victoria. The first paper from that unit appeared in an earlier issue of Brain for the same year, adding to the classical literature on injuries to nerves that had began with the observations of Silas Weir Mitchell at Gettysburg during the American Civil War.
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= superficial radial fibres; S = supinator fibres. + = extensor carpi radialis brevis fibres; X = extensor carpi radialis longus fibres; * = extensores carpi radialis fibres; 
= brachioradialis fibres; 
= brachialis fibres.Cambridge
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