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Cutaneous afferents provide a neuronal population vector that encodes the orientation of human ankle movements


Jean-Marc Aimonetti; Valérie Hospo;, Jean-Pierre Roll; Edith Ribot-Ciscar.

The aim of this study was to analyse the directional coding of two-dimensional limb movements by cutaneous afferents from skin areas covering a multidirectional joint, the ankle. The activity of 89 cutaneous afferents was recorded in the common peroneal nerve, and the mean discharge frequency of each unit was measured during the outward phase of ramp and hold movements imposed in 16 different directions. Forty-two afferents responded to the movements in the following decreasing order (SA2, n = 24/27; FA2, n = 13/17; FA1, n = 3/24; SA1, n = 2/21). All the units activated responded to a specific range of directions, defining their ‘preferred sector', within which their response peaked in a given direction, their ‘preferred direction'. Based on the distribution of the preferred directions, two populations of afferents, and hence two skin areas were defined: the anterior and the external lateral parts of the leg. As the directional tuning of each population was cosine shaped, the neuronal population vector model was applied and found to efficiently describe the movement direction encoded by cutaneous afferents, as it has been previously reported for muscle afferents. The responses of cutaneous afferents were then considered with respect to those of the afferents from the underlying muscles, which were previously investigated, and an almost perfect matching of directional sensitivity was observed. It is suggested that the common movement-encoding characteristics exhibited by cutaneous and muscle afferents, as early as the peripheral level, may facilitate the central co-processing of their feedbacks subserving kinaesthesia. Previous Section Next Section Kinaesthesia involves multiple sensory messages arising from mechanoreceptors located in the joints themselves and in all the surrounding tissues. The relative contributions of joint, muscle and cutaneous information to kinaesthesia are still a much-debated issue because the corresponding receptors are concurrently subjected to mechanical constraints during the performance of movements (see Gandevia, 1996). Joint inputs contribute to kinaesthesia, as intracapsular anaesthesia impairs subjects' ability to evaluate the velocity of passive finger movements (Ferrell et al. 1987), and intraneural microstimulation applied to joint afferents induces illusory sensations of joint displacement (Macefield et al. 1990). The information arising from these receptors might, however, operate only at the extremes of joint displacement ranges (Burke et al. 1988; Clark et al. 1989). As far as the muscle inputs are concerned, nerve block reversibly removing these inputs impairs the subjects' ability to detect passive movements (Clark et al. 1985), while vibration induces clearly perceptible illusory sensations of movement (Goodwin et al. 1972) by strongly activating primary muscle spindle endings, as shown by microneurographic recordings performed on humans (Burke et al. 1976a,b; Roll & Vedel, 1982; Roll et al. 1989). Tendon vibration causes the sensation of an illusory movement, the direction of which is that of the real movement which would have stretched the receptor-bearing muscle. It was initially suggested that the sensory messages arising from the lengthened muscle contributed mainly to kinaesthesia (Roll & Vedel, 1982). More recently it was established, however, that muscle feedback originating not only from the antagonist-lengthened muscle, but also from the agonist muscle, co-contribute to the encoding of unidirectional movements (Ribot-Ciscar & Roll, 1998). This assumption was then extended to the case of multidirectional movements, based on the finding that all the muscle spindle information arising from all the muscles surrounding a joint contributes together to the coding of two-dimensional movement parameters under both passive and active conditions (Bergenheim et al. 2000; Roll et al. 2000; Jones et al. 2001; Ribot-Ciscar et al. 2002, 2003). Cutaneous information seems to also contribute to kinaesthesia since anaesthesia of the digital nerves impairs finger-movement detection (Brown et al. 1954; Gandevia & McCloskey, 1976; Refshauge et al. 1998). In addition, transcutaneous electrical stimulation applied to the hand induces illusory sensations of movement (Collins & Prochazka, 1996), as does stretching of the skin over the hand (Edin & Abbs, 1991; Edin & Johansson, 1995; Collins & Prochazka, 1996), elbow and knee joints (Collins et al. 2005). Lastly, vibratory stimulation applied to the plantar sole, which was liable to stimulate the cutaneous mechanoreceptors, was found to induce illusory perceptions of orientated whole-body leaning (Roll et al. 2002). Although muscle spindle and tactile afferent feedbacks contribute separately to kinaesthesia, evidence has been accumulated during the last decade that these sensory inputs are co-processed and contribute to movement perception (Collins et al. 2000) and erect stance maintenance (Kavounoudias et al. 2001). By combining muscle-vibration and skin-stretching stimuli, Collins et al. (2005) observed, for example, that the amplitude of the illusory movements induced was larger when muscle spindle and tactile receptors were activated simultaneously rather than separately. These data add to the findings made in the pioneer study by Collins et al. (2000) showing that cutaneous feedback from the fingers does not facilitate the sensations resulting from muscle receptor activation, but may actually help the subject to identify which finger is moving (see also Refshauge et al. 2003). If integrated muscle and cutaneous inputs provide kinaesthetic information, these two sensory modalities can be expected to share some general encoding characteristics. As regards the direction of movements and muscle proprioceptive information, it was recently established that each muscle surrounding a particular joint encodes a specific range of movement directions, which has been called the muscle's preferred sensory sector, and particularly one movement direction, its preferred sensory direction (Bergenheim et al. 2000). This study showed in addition that movement direction is encoded by populations of afferents originating from all the muscles subjected to deformation, in keeping with the neuronal population vector model (Georgopoulos et al. 1986). Since this population-encoding process was also found to reflect the directional encoding of forces applied to periodontal and finger-tip mechanoreceptors (Trulsson et al. 1992; Birznieks et al. 2001), the aim of the present study was to determine whether cutaneous afferents with receptive fields surrounding a multidirectional joint, the ankle, encode the direction of two-dimensional movements in keeping with the same population vector model.

Palavras-chave: Cutaneous afferents, orientation of human ankle movements

J.-M. Aimonetti: Laboratoire de Neurobiologie Humaine. UMR 6149 Université de Provence – CNRS Pôle 3C – Case B Centre St Charles 3 Place Victor Hugo 13331 Marseille Cedex 03 France.? Email: aimon@up.univ-mrs.fr