Proprioceptive population coding of two-dimensional limb movements in humans: I. Muscle spindle feedback during...

The proprioceptive coding of multidirectional ankle joint movements was investigated, focusing in particular on the question as to how accurately the direction of a movement is encoded when all the proprioceptive information from all the muscles involved in the actual movement is taken into account. During ankle movements imposed on human subjects, the activity of 30 muscle spindle afferents originating in the extensor digitorum longus, tibialis anterior, extensor hallucis longus and peroneus lateralis muscles was recorded from the lateral peroneal nerve using the microneurographic technique. In the first part of the study, it was proposed to investigate whether muscle spindle afferents have a preferred direction, as previously found to occur in the case of cortical cells, and to analyze the neural coding of the movement trajectories using a "population vector model." This model is based on the idea that neuronal coding can be analyzed in terms of a series of vectors, each based on specific movement parameters. In the present case, each vector gives the mean contribution of a population of muscle spindle afferents within one directionally tuned muscle. A given population vector points in the "preferred sensory direction" of the muscle to which it corresponds, and its length is the mean frequency of all the afferents within that muscle. Our working hypothesis was that the sum of these weighted vectors points in the same direction as the ongoing movement. The results show that each muscle spindle afferent, and likewise each muscle, has a specific preferred sensory direction, as well as a preferred sensory sector within which it is capable of sending sensory information to the central nervous system. Interestingly, the results also demonstrate that the preferred directions are the same as the directions of vibration-induced illusions. In addition, the results show that the neuronal population vector model describes the multipopulation proprioceptive coding of spatially oriented 2D limb movements, even at the peripheral sensory level, based on the sum vectors calculated from all the muscles involved in the movement. In an accompanying paper, the coding of more complex 2D movements such as those involved in drawing rectilinear and curvilinear geometrical shapes was investigated.