New functional and anatomical aspects of the organisation of human peripheral nerve

Abstract

The functional topography of peripheral nerves has been studied by various indirect electrophysiological and histological methods. Even though some studies have suggested the presence of a somatotopical arrangement of nerve fibres, the prevailing view is that a random distribution of nerve fibres develops in the nerve due to the repeated rearrangement of nerve fascicles along their centripetal course. From observations of functional nerve regeneration after nerve suture and the existence of a somatotopic and modality segregation of central neurons, the random fibre organisation can be questioned. To study the topographical organisation of nerve fibres in sensory nerve fascicles in humans we used a more selective technique that reflects the properties of neighbouring fibres more accurately than previously used methods.

Concentric microneurography electrodes were used to impale sensory nerve fascicles in conscious, healthy human volunteers. In the majority of experiments the electrode was percutaneosly positioned into the median nerve at elbow level with slightly varying locations up till 10 cm proximal to the elbow joint or at the wrist. In some experiments the ulnar nerve was explored at the elbow. The properties of the recorded potentials were described at each recording position. The neural signals could be classified into multiunit activity, the activity of single units derived from different classes of receptors innervated by myelinated nerve fibres and unmyelinated C-afferents. Spontaneous or evoked activity from efferent sympathetic C-fibers could be also distinguished. The topographical relationship of neighbouring nerve fibres was described in two ways. First, neural responses to various electrical and tactile stimuli applied to the receptive field in a stable recording position were analysed. Second, the receptive fields and properties of the neural activity recorded from subsequent positions of the electrode in the explored fascicle were assessed.

The data from 120 experiments were analysed and evaluated by statististics which formulated hypothetical stochastic models assuming different combinations of fibre organisation and distribution of nodes of Ranvier between neighbouring intrafascicular fibres. For the model assuming modality segregation of the myelinated afferent A-fibres and clustering of nodes, the best correlation was found between the simulated and experimental data. The intrafascicular arrangement of efferent sympathetic and C-afferents was evaluated and the fibre types were found to be segregated. Neighbouring afferent myelinated fibres with the same modality also had a clear tendency to have neighbouring receptive fields and a maintained somatotopical distribution in the nerve fascicle. Adjacent or overlapping receptive fields for afferents of the various modalities could be demonstrated. The observed fibre organisation in peripheral sensory nerves can offer guidance for nerve repair techniques and serve as a basis for better understanding of sensory transmission under normal conditions and pathology in different neuropathies.