Cutaneous Receptors Contribute to Kinesthesia at the Index Finger, Elbow, and Knee D. F. Collins, 1,3 K. M. Refshauge, 2,3 G. Todd, 3 and S. C. Gandevia 3 1 Human Neurophysiology Laboratory, Faculty of Physical Education and Recreation, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada; 2 University of Sydney and 3 Prince of Wales Medical Research Institute and University of New South Wales, Sydney, New South Wales, Australia Submitted 23 February 2005; accepted in final form 14 May 2005 Collins, D. F., K. M. Refshauge, G. Todd, and S. C. Gandevia. Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J Neurophysiol 94: 1699 –1706, 2005. First pub- lished May 25, 2005; 10.1152/jn.00191.2005.. The neural mecha- nisms underlying the sense of joint position and movement remain controversial. While cutaneous receptors are known to contribute to kinesthesia for the fingers, the present experiments test the hypothesis that they contribute at other major joints. Illusory movements were evoked at the interphalangeal (IP) joints of the index finger, the elbow, and the knee by stimulation of populations of cutaneous and muscle spindle receptors, both separately and together. Subjects matched perceived movements with voluntary movements of homologous joints on the contralateral side. Cutaneous receptors were activated by stretch of the skin (using 2 intensities of stretch) and vibration activated muscle spindle receptors. Stimuli were designed to activate receptors that discharge during joint flexion. For the index finger, vibration was applied over the extensor tendons on the dorsum of the hand, to evoke illusory metacarpophalangeal (MCP) joint flexion, and skin stretch was delivered around the IP joints. The strong skin stretch evoked the illusion of flexion of the proximal IP joint in 6/8 subjects (12  5°, mean  SE). For the group, strong skin stretch delivered during vibration increased the perceived flexion of the proximal IP joint by eight times with a concomitant decrease in perceived flexion of the MCP joint compared with vibration alone (P  0.05). For the elbow, vibration was applied over the distal tendon of triceps brachii and skin stretch over the dorsal forearm. When delivered alone, strong skin stretch evoked illusory elbow flexion in 5/10 subjects (9  4°). Simultaneous strong skin stretch and vibration increased the illusory elbow flexion for the group by 1.5 times compared with vibration (P  0.05). For the knee, vibration was applied over the patellar tendon and skin stretch over the thigh. Skin stretch alone evoked illusory knee flexion in 3/10 subjects (8  4°) and when delivered during vibration, perceived knee flexion increased for the group by 1.4 times compared with vibration (P  0.05). Hence inputs from cuta- neous receptors, muscle receptors, and combined inputs from both receptors likely subserve kinesthesia at joints throughout the body. INTRODUCTION Kinesthesia, the sense of position and movement, is a vital component of proprioception, and its disturbance markedly impairs voluntary movement (e.g., Cole 1995; Rothwell et al. 1982). However, understanding the mechanisms that mediate this ability has long been controversial (for review, see Mc- Closkey 1978). For more than 100 years, opinion swayed between an important role for central signals associated with the command to move (Helmholtz 1867; von Holst 1954) and peripheral feedback from sensory receptors (Sherrington 1900). During the latter half of the 20th century, the balance tipped toward a peripheral origin, at least for perception of limb movements, and the focus then shifted to identification of which sensory receptor predominated. Arguments for receptors located in muscle (Goodwin et al. 1972; Matthews 1977; McCloskey et al. 1983), joints (Boyd and Roberts 1953; Ferrell et al. 1987; Gelfan and Carter 1967), and the skin (Edin and Abbs 1991; Gandevia and McCloskey 1976; Provins 1958) have been advanced, but during the last 30 years, a consensus has developed that feedback from muscle spindle receptors is the most important source of proprioceptive information (e.g., Gandevia 1996; Kandel et al. 2000; Smetacek and Mechsner 2004). This idea stemmed originally from the finding of pow- erful illusions of position and movement when muscle spindles were activated by tendon vibration (Goodwin et al. 1972) but has been corroborated using a variety of methods (e.g., Gan- devia 1985; Gandevia and McCloskey 1976; McCloskey et al. 1983). Despite this, proponents for a role for cutaneous recep- tors remained, initially based on clinical observations during reconstructive surgery (Moberg 1972, 1983) but also from experiments in which cutaneous feedback was removed by anesthesia (e.g., Gandevia and McCloskey 1976; Moberg 1983; Refshauge et al. 2003). Subsequent microneurographic studies lent support to a potential cutaneous contribution to kinesthesia; cutaneous receptors in the hand (Edin 1992, 2004; Edin and Abbs 1991; Grill and Hallet 1995; see also Burke et al. 1988; Hulliger et al. 1979) and around the knee (Edin 2001) can provide information about the position and movement of nearby joints. Although joint receptors probably contribute (Ferrell et al. 1987), this has been difficult to demonstrate and the lack of a major proprioceptive deficit on removal of joint receptor feedback has contributed to the diminishing attention they receive. Just as the signaling of arterial pressure by baroreceptors does not mean that arterial pressure must be perceived, the fact that cutaneous receptors provide adequate signals of joint movement does not ensure that the CNS uses this afferent signal for sensation of joint movement. Two groups assessed whether cutaneous receptors contribute to the perception of movements of the fingers (Collins and Prochazka 1996; Edin and Johansson 1995). Both found that stimulation of cutaneous receptors of the hand produced illusions of finger movement. Address for reprint requests and other correspondence: D. F. Collins, E 435 Van Vliet Centre, Centre for Neuroscience, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, Alberta T6G 2H9, Canada (E-mail: dave.collins@ualberta.ca). The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. J Neurophysiol 94: 1699 –1706, 2005. First published May 25, 2005; 10.1152/jn.00191.2005. 1699 0022-3077/05 $8.00 Copyright © 2005 The American Physiological Society www.jn.org