Cutaneous afferents provide information about knee joint movements in humans

Abstract

1. Neurophysiological evidence that afferent information from skin receptors is important for proprioception has been gathered mainly in experiments relating to the human hand and finger joints. To investigate if proprioceptive information is also provided by skin mechanoreceptor afferents from skin areas related to large joints of postural importance, microneurography recordings were obtained in humans from skin afferents in the lateral cutaneous femoral nerve to study their responses to knee joint movements. 2. Data were collected from 60 sequentially recorded afferents from slowly (n = 23) and fast (n = 6) adapting low-threshold mechanoreceptors, hair follicle receptors (n = 24), field receptors (n = 1) and C mechanoreceptors (n = 6). Fascicular recordings showed that the lateral cutaneous femoral nerve supplies extensive areas of the thigh: from 5-10 cm below the inguinal ligament down to below and lateral to the knee joint; accordingly, the afferents originated in receptors located in wide areas of the human thigh. 3. All afferents from fast and slowly adapting low-threshold mechanoreceptors, as well as C mechanoreceptors, responded to manually applied skin stretch. In contrast, the same stimulus elicited, at most, feeble responses in hair follicle receptors. 4. Qualitative and quantitative analyses of the responses of a subset of afferents revealed that in particular slowly adapting afferents effectively encode both static and dynamic aspects of passively imposed knee joint movements. 5. It was concluded that receptors in the hairy skin of humans can provide high-fidelity information about knee joint movements. A previously undefined type of slowly adapting receptor (SA III) seemed particularly suited for this task whereas this does not seem to be the case for either hair follicle receptors or C mechanoreceptors.

Figure 2. Knee joint movements and associated neural responses in SA III units

The instantaneous discharge rate was fitted by a linear combination of the angular velocity and the knee joint angle and shown with dotted lines superimposed on the recorded discharge rate (unit 7-1 in C responded to both flexion and extension). Insets show unitary spikes superimposed for the whole displayed time window. The scales of knee joint position and angular velocity were reversed for unit 15-3 (in B) to make it easier to compare them with the unit’s neural response that increased with knee extension rather than flexion. The knee joint angle was defined as zero when the knee was held in a fully extended but not hyperextended position. Note separate time scales in D.

Figure 3. Recordings from C mechanoreceptors

Recordings from two C mechanoreceptive afferents with receptive fields just proximal to the patella and on the lateral proximal thigh (schematic inset). As illustrated for unit 5-1, these receptors responded vigorously to mechanical stimulation but fatigued rapidly (A), and showed low conduction velocities (B). Feeble responses with long delays were observed in response to knee joint movements (C and D). Recordings from two C mechanoreceptive afferents with receptive fields just proximal to the patella and on the lateral proximal thigh (schematic inset). As illustrated for unit 5-1, these receptors responded vigorously to mechanical stimulation but fatigued rapidly (A), and showed low conduction velocities (B). Feeble responses with long delays were observed in response to knee joint movements (C and D).

Figure 1. Fascicular and receptive fields

A, fascicular receptive fields mapped by light tactile stimuli while recording multi-unit neural activity in microneurographic recordings in three subjects. B, location of the centre of all receptive fields for slowly and fast adapting afferents and C mechanoreceptive afferents. There was no sign of increased receptor densities close to the knee joint.