Proprioceptive population coding of limb position in humans
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The present study investigates the coding of positions reached in a two-dimensional space by populations of muscle spindle afferents. The unitary activity of 35 primary muscle spindle afferents originating from the tibialis anterior, extensor digitorum longus, extensor hallucis longus, and peroneus lateralis muscles were recorded from the common peroneal nerve by the microneurographic technique. The steady mean frequency of discharge was analyzed during 16 passively maintained positions of the tip of the foot. These positions were equally distant from and circularly arranged around the "neutral" position of the ankle. The results showed that a same position of the foot was differently coded depending on whether it was maintained for several seconds or whether it was attained after a movement. Muscle spindle activity was increased or decreased, respectively, when the previous movement lengthened or shortened the parent muscle; the magnitude of change in activity depended on the amount of lengthening or shortening in relation to movement direction. Each muscle surrounding the ankle joint was shown to encode the different spatial positions following a directional tuning curve. Data were analyzed by using the "neuronal population vector model". This model consists of calculating population vectors representing the mean contribution of each muscle population of afferents to the coding of a particular position, and by finally calculating a sum vector. The direction of the sum vector was shown to accurately describe the direction of a given maintained position compared to the initial position. We conclude that muscle spindle position coding is based on afferent information coming from the whole set of muscles crossing a given joint. A given spatial position is associated with a stable muscle afferent inflow where each muscle makes an oriented and weighted contribution to its coding.
KeywordsProprioception Muscle afferents Sensory coding Position sensitivity Microneurography
This work was supported by grants from CNRS, INSERM, "Marseille Provence Métropole", the Swedish Council for Work Life Research, and the Swedish Foundation for International Cooperation in Research and Higher Education.
- Batschelet E (1981) Circular statistics in biology. Academic Press, LondonGoogle Scholar
- Bergenheim M, Roll J-P, Ribot-Ciscar E (1999) Microneurography in humans. In: Windhorst U, Johansson H (eds) Modern techniques in neuroscience research. Springer, Berlin Heidelberg New York, pp 801–819Google Scholar
- Clark FJ, Burgess RC, Chapin JW, Lipscomb WT (1985) Role of intramuscular receptors in the awareness of limb position. J Neurophysiol 54:1529–1540Google Scholar
- Gandevia SC, McCloskey DI, Burke D (1992) Kinaesthetic signals and muscle contraction. Trends Neurosci 15:62–65Google Scholar
- Georgopoulos AP (1990) Neural coding of the direction of reaching and a comparison with saccadic eye movements. Cold Harb Symp Quant Biol 55:849–859Google Scholar
- Georgopoulos AP, Caminiti R, Kalaska JF, Massey JT (1983) Spatial coding of movement: a hypothesis concerning the coding of movement direction by motor cortical populations. Exp Brain Res Suppl 7:327–336Google Scholar
- Granit R, Homma S (1959) The discharge to maintained stretch of spindles in slow and fast muscle of rabbit. Acta Physiol Scand 46:165–173Google Scholar
- McCloskey DI, Gandevia S, Potter EK, Colebatch JG (1983) Muscle sense and effort: motor commands and judgements about muscle contractions. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Raven press, New York, pp 151–167Google Scholar