This article was downloaded by: [Universite Laval] On: 26 June 2014, At: 09:06 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Journal of Motor Behavior Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/vjmb20
Proprioception, Tensegrity, and Motor Control Simon C. Gandevia
a
a
Neuroscience Research Australia and University of New South Wales , Sydney, Australia Published online: 14 Mar 2014.
To cite this article: Simon C. Gandevia (2014) Proprioception, Tensegrity, and Motor Control, Journal of Motor Behavior, 46:3, 199-201, DOI: 10.1080/00222895.2014.883807 To link to this article: http://dx.doi.org/10.1080/00222895.2014.883807
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Motor Behavior, Vol. 46, No. 3, 2014 C Taylor & Francis Group, LLC Copyright
COMMENTARY
Proprioception, Tensegrity, and Motor Control Simon C. Gandevia Neuroscience Research Australia and University of New South Wales, Sydney, Australia.
length changes and their time derivatives (e.g., Matthews, 1972). Traditionally muscle spindles are considered to be in parallel with the nonspindle tissues (i.e., extrafusal muscle). Hence, they would have a simple path for the distribution of stress and be able to respond faithfully to muscle length changes. Less well known is that some spindles (including in human muscles) are in series with the extrafusal muscle and its connective tissue matrix such that their local deformation, and hence their signaling, must be more complex (see Burke, Aniss, & Gandevia, 1987). Consequently, the encoding of length disturbances by a population of spindle endings does not translate into a ruler-like, Newtonian, measure of the length of the muscle-tendon unit (e.g., Dimitriou & Edin, 2008). If the purpose of spindle populations were to provide such a measure then some additional problems considered to varying degrees by Turvey and Fonseca (2014) require solving. First, the receptors are not uniformly distributed within the muscle and their distribution and density varies between muscles in ways that have not yet been satisfactorily resolved. Spindle density (expressed as spindle number per muscle weight or number of muscle fibers) is not directly linked to the capacity to perform fine-grained contractions (for details, see Gandevia & Burke, 1992). Whether some other movement parameter is so linked remains a speculation. There is no a priori reason why spindle density should be the primary measure to link to function when theoretically one stretch receptor in parallel with the extrafusal muscle would do. The location of spindles (and other specialized receptors such as Golgi tendon organs) within muscles has also remained a vexed issue. The proposal here that they reside at transitional zones between tissue regions of different viscoelastic properties is testable. Furthermore, if confirmed, it represents a fundamental pattern laid down in development. At least in human skeletal muscle, the idea that spindles may be rich in regions of type 1 (oxidative, low voluntary threshold) muscle fibers is not well supported. In a similar vein, we do not know the fundamental basis for the distribution of tendon organs. Second, the history dependence of the muscle and connective tissue net (MCS) to stirring reveals its thixotropic properties. While this property resides broadly in the MCS and can be demonstrated to alter human muscle properties (e.g., Lakie & Robson, 1988; see Figure 13 in Turvey & Fonseca, 2014), it is particularly prominent in the actin-myosin interactions within the muscle spindle’s intrafusal fibers (Proske,
ovements for breathing, locomotion, and feeding are critical for survival, but how they are controlled by the CNS is poorly understood. It has long been recognized that sensory information from receptors in many tissues is required for accurate movements. Such information may be transduced by receptors in the skin, joint and muscles and their associated connective tissues. Additional information about the body’s relation to the external environment derives from the vestibular apparatus, while the eye and ear provide further data. This information is considered to be compiled into a fluid functional brain map or representation of the body and its parts, a map that is consulted to plan and execute movements. Multisensory inputs and planning are also involved in the deceptively simple task of standing (e.g., Loram, Magnaaris, & Lakie, 2005). In their special review, Turvey and Fonseca (2014) tackle the medium of haptic perception on a broad dimensional scale, from subcellar components to the whole organism. They go on to propose that tensigrity, a fundamental structural property based on efficient deployment of tension and compression elements, is a unifying concept, again over a broad scale of size. The review by Turvey and Fonseca (2014) performs the helpful task of suggesting some much-needed linkages across different fields, from structural biology to neuroscience. Not surprisingly, the attempt is fraught with dangers but nonetheless it raises some important questions. I consider briefly some of the linkages and some of the controversies.
Downloaded by [Universite Laval] at 09:06 26 June 2014
M
Some Peripheral Issues An important emphasis is the functional relation between the micro and macro properties of the musculoskeletal system, and perhaps, the authors would argue, even the body as a whole. For example, it is good to be reminded that the basic mechanism of hearing should not be viewed solely in a narrow focus from the molecular behavior of the cochlear inner hair cells to the properties of the cochlear nerve fibers and then their central projections. Instead, it is better, at a more ecological level (e.g., Dusenbery, 1992) to consider the properties of the tissues in which the hair cells are embedded from the basilar membrane, back through the bones of the middle ear and the muscles which dampen their effects, to the pinna and ultimately the types of environmental vibration that are being transduced. Of course this concept can be extended to the main classes of proprioceptors. Here the muscle spindle offers some insight. This structure resides within mammalian muscles and has seemingly complex afferent and efferent connections with the central nervous system. It is well known that primary and secondary muscle spindle endings encode
Correspondence address: Simon C. Gandevia, Neuroscience Research Australia, Barker Street, Randwick, Sydney NSW 2031, Australia. e-mail: [email protected] 199
Downloaded by [Universite Laval] at 09:06 26 June 2014
S. C. Gandevia
Morgan, & Gregory, 1993). Hence, the fusimotor drive to these fibers that accompanies voluntary activity combined with changes in length of the muscle can leave its muscle spindles in a tight or more loose configuration, despite the muscle-tendon unit staying at the same length. Spindle firing is high under the tight condition and low or absent under the loose condition. This alters proprioception as the muscle will be perceived as long or short depending on the firing rate of its spindles, and it will affect the sensory response of the muscle to perturbations and hence its reflex and volitional output (for a review, see Proske & Gandevia, 2012). Intrafusal thixotropy and the variability in the response of human muscle spindles from the same muscle to a similar length change raises difficulty for the claim that the MCS should be considered a homogenous isotropic medium. The various pathways for force transfer within and between muscles and other structures (i.e., intramuscular, intermuscular, and extramuscular force transmission) are contentious. However, since the pioneering work of Street (1983) on frog muscle and subsequently by Huijing (2003, 2009; for references, see Turvey & Fonseca, 2014) on different mammalian preparations, there can be no doubt of their existence. What remains is to quantify the size of the effects and the circumstances under which they occur. At least for the human triceps surae, with the common insertion of the gastrocnemii and soleus into the Achilles tendon, there is no argument about the presence of intermuscular force transmission between medial gastrocnemius and soleus, but the available evidence suggests that the magnitude of the effect would not produce a big change in the passive length-tension curve of the ankle plantarflexors (Tian, Herbert, Hoang, Gandevia, & Bilston, 2012). In the human upper limb, there are dramatic examples of effective disconnection of muscles from their insertions on the distal phalanx depending on the length of their nearby neighbors (for details, see Van Duinen & Gandevia, 2011) such that the active contraction of flexor digitorum profundus to one finger can generate no force at its insertion. It is an example of “no force” transmission and a dramatic demonstration of the importance of the MCS for movement. However, for the long finger flexors and extensors operating within their common length ranges, the forces produced by their single motor units do not spillover to generate much force via neighboring tendons (for references, see Van Duinen & Gandevia, 2011). This provides some simplification at the level of the periphery for selective force control in the fingers. However, we are only just beginning to tackle some of deeper issues of movement control that are engendered by a realization that there is a spectrum of degrees of nonlinear force transmission. Some Central Issues If we accept that the central nervous system has to integrate the neural signals it receives to control movement, both moment-to-moment as well as over short and long time scales (e.g., for learning a skill, for adapting to limb growth), 200
then how is this achieved? This proposition is not necessarily accepted by the authors, and some theoretical limits to the coding are raised. My response is that the brain has evolved methods that do solve the coding complexity for haptic and proprioceptive perception. Thus, the brain can generate a range of possible scenarios and test them for consistency against available sensory information. This scenario-based testing model explains many proprioceptive and visual illusions (e.g., Gregory, 2009). Hence, artificially increased firing of muscle spindles (produced by vibratory or electrical stimulation of say elbow flexors) can produce a sense that the elbow joint is moving into extension, and that it occupies a more extended position, and that the body part that the hand is holding (say the nose) is lengthened. Presumably comparable solutions are available centrally for stimuli, which do not necessarily reach perception (e.g., Luu et al., 2012). An issue that has been central to many motor control theories since the time of Helmholtz, namely the differentiation of stimuli that are self-generated from those generated by the external environment, was not included in the analysis by Turvey and Fonseca of haptic perception. Clearly, a scenariobased model, or a prediction-based model, of which many have been described is required (e.g., Bays & Wolpert, 2007; Proske & Gandevia, 2012). The variety of ways in which such models need to operate has recently been described for limb movements (Walsh, Taylor, & Gandevia, 2011) and also eye movements (Whitham et al., 2010). It is difficult to see how an overarching tensigrity-based view of the peripheral structures involved in production of movement (i.e., muscles) and the consequence of movement (i.e., sensory input) can explain the differentiation noted previously. Furthermore, there are major contributions from centrally- generated signals of motor command to proprioception, both for signals of limb position and movement (Gandevia, Smith, Crawford, Proske, & Taylor, 2006; Walsh, Gandevia, & Taylor, 2010) and for signals of force (e.g., Gandevia, 1987; cf. Luu, Day, Cole, & Fitzpatrick, 2011; see also Proske & Gandevia, 2012). Concluding Comment The review by Turvey and Fonseca (2014) is stronger in exposing the peripheral mechanisms that are required for haptic, kinesthetic, or proprioceptive judgments than it is in delineating the central processes that must underlie perception and action. This should remind us that for too long the physiologists, psychologists, clinicians, and others have overemphasized the apparently separate perceptual (and other) effects due to activity in one anatomical class of receptor (i.e., those in the skin, joints, or muscles) rather than the orchestrated effects that their usual combination evokes. This likely arose from the anatomists’ natural desire to subdivide musculoskeletal tissues into muscle, joint, tendon, and aponeurosis. Furthermore, we have not broken out from the Sherringtonian terminology of proprioception and its relatives (exteroception, enteroception), Bastian’s earlier but enduring versions of kinesthesis, and the simplistic clinical term joint position Journal of Motor Behavior
Proprioception, Tensegrity, and Motor Control
sense. Hopefully a better terminology will emerge, which could helpfully link with the more encompassing view of the muscle and connective tissue network. Time will tell whether this network is the ultimate medium for haptic sensation. FUNDING The author’s research is supported by the National Health and Medical Research Council (of Australia).
Downloaded by [Universite Laval] at 09:06 26 June 2014
REFERENCES Bays, P. M., & Wolpert, D. M. (2007). Computational principles of sensorimotor control that minimize uncertainty and variability. Journal of Physiology, 578, 387–396. Burke, D., Aniss, A. M., & Gandevia, S. C. (1987). In-parallel and in-series behavior of human muscle spindle endings. Journal of Neurophysiology, 58, 417–426. Dimitriou, M., & Edin, B. B. (2008). Discharges in human muscle spindle afferents during a key-pressing task. Journal of Physiology, 586, 5455–5470. Dusenbery, D. B. (1992). Sensory ecology: How organisms acquire and respond to information. New York, NY: W. H. Freeman. Gandevia, S. C. (1987). Roles for perceived motor commands in motor control. Trends in Neurosciences, 10, 81–85. Gandevia, S. C., & Burke, D. (1992). Does the nervous system depend on kinesthetic information to control natural limb movements. Behavioral Brain Sciences, 15, 614–632 and 815–819. Gandevia, S. C., Smith, J. L., Crawford, M., Proske, U., & Taylor, J. L. (2006). Motor commands contribute to human position sense. Journal of Physiology, 571, 703–710. Gregory, R. (2009). Seeing through illusions. Oxford, England: Oxford University Press. Huijing, P. A. (2003). Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exercise and Sport Sciences Reviews, 31, 167–175. Huijing, P. A. (2009). Epimuscular myofascial force transmission: A historical review and implications for new research. Journal of Biomechanics, 42, 9–21.
2014, Vol. 46, No. 3
Lakie, M., & Robson, L. G. (1988). Thixotropic changes in human muscle stiffness and the effects of fatigue. Quarterly Journal of Experimental Physiology, 73, 487–500. Loram, I. D., Maganaris, C. N., & Lakie, M. (2005). Active, nonspring-like muscle movements in human postural sway: how might paradoxical changes in muscle length be produced? Journal of Physiology, 564, 281–293. Luu, B. L., Day, B. L., Cole, J. D., & Fitzpatrick, R. C. (2011). The fusimotor and reafferent origin of the sense of force and weight. Journal of Physiology, 589, 3135–3147. Luu, B. L., Inglis, J. T., Huryn, T. P., Van der Loos, H. F., Croft, E. A., & Blouin, J. S. (2012). Human standing is modified by an unconscious integration of congruent sensory and motor signals. Journal of Physiology, 590, 5783–5794. Matthews, P. B.C. (1972). Mammalian muscle receptors and their central actions. London, England: Arnold. Proske, U., & Gandevia, S. C. (2012). The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiological Reviews, 92, 1651–1697. Proske, U., Morgan, D. L., & Gregory, J. E. (1993). Thixotropy in skeletal muscle and in muscle spindles: a review. Progress in Neurobiology, 41, 705–721. Street, S. F. (1983). Lateral transmission of tension in frog myofibers. Journal of Cellular Physiology, 114, 346–364 Tian, M., Herbert, R. D., Hoang, P., Gandevia, S. C., & Bilston, L. E. (2012). Myofascial force transmission between the human soleus and gastrocnemius muscles during passive knee motion. Journal of Applied Physiology, 113, 517–523. Turvey, M. T., & Fonseca, S. T. (2014) The medium of haptic perception: A tensegrity hypothesis. Journal of Motor Behavior, 46, 143–187. Van Duinen, H., & Gandevia, S. C. (2011). Constraints for control of the human hand. Journal of Physiology, 589, 5583–5593. Walsh, L. D., Gandevia, S. C., & Taylor, J. L. (2010). Illusory movements of a phantom hand grade with the duration and magnitude of motor commands. Journal of Physiology 588, 1269– 1280. Walsh, L. D., Taylor, J. L., & Gandevia, S. C. (2011). Overestimation of force during matching of externally generated forces. Journal of Physiology, 589, 547–557. Whitham, E. M., Fitzgibbon, S. P., Lewis, T. W., Pope, K. J., Delosangeles, D., Clark, C. R., . . . Hughby, J. O. (2011). Visual experiences during paralysis. Frontiers in Human Neuroscience 5, 160. doi:10.3389/fnhum.2011.00160
201
Journal of Motor Behavior Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/vjmb20
Proprioception, Tensegrity, and Motor Control Simon C. Gandevia
a
a
Neuroscience Research Australia and University of New South Wales , Sydney, Australia Published online: 14 Mar 2014.
To cite this article: Simon C. Gandevia (2014) Proprioception, Tensegrity, and Motor Control, Journal of Motor Behavior, 46:3, 199-201, DOI: 10.1080/00222895.2014.883807 To link to this article: http://dx.doi.org/10.1080/00222895.2014.883807
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Motor Behavior, Vol. 46, No. 3, 2014 C Taylor & Francis Group, LLC Copyright
COMMENTARY
Proprioception, Tensegrity, and Motor Control Simon C. Gandevia Neuroscience Research Australia and University of New South Wales, Sydney, Australia.
length changes and their time derivatives (e.g., Matthews, 1972). Traditionally muscle spindles are considered to be in parallel with the nonspindle tissues (i.e., extrafusal muscle). Hence, they would have a simple path for the distribution of stress and be able to respond faithfully to muscle length changes. Less well known is that some spindles (including in human muscles) are in series with the extrafusal muscle and its connective tissue matrix such that their local deformation, and hence their signaling, must be more complex (see Burke, Aniss, & Gandevia, 1987). Consequently, the encoding of length disturbances by a population of spindle endings does not translate into a ruler-like, Newtonian, measure of the length of the muscle-tendon unit (e.g., Dimitriou & Edin, 2008). If the purpose of spindle populations were to provide such a measure then some additional problems considered to varying degrees by Turvey and Fonseca (2014) require solving. First, the receptors are not uniformly distributed within the muscle and their distribution and density varies between muscles in ways that have not yet been satisfactorily resolved. Spindle density (expressed as spindle number per muscle weight or number of muscle fibers) is not directly linked to the capacity to perform fine-grained contractions (for details, see Gandevia & Burke, 1992). Whether some other movement parameter is so linked remains a speculation. There is no a priori reason why spindle density should be the primary measure to link to function when theoretically one stretch receptor in parallel with the extrafusal muscle would do. The location of spindles (and other specialized receptors such as Golgi tendon organs) within muscles has also remained a vexed issue. The proposal here that they reside at transitional zones between tissue regions of different viscoelastic properties is testable. Furthermore, if confirmed, it represents a fundamental pattern laid down in development. At least in human skeletal muscle, the idea that spindles may be rich in regions of type 1 (oxidative, low voluntary threshold) muscle fibers is not well supported. In a similar vein, we do not know the fundamental basis for the distribution of tendon organs. Second, the history dependence of the muscle and connective tissue net (MCS) to stirring reveals its thixotropic properties. While this property resides broadly in the MCS and can be demonstrated to alter human muscle properties (e.g., Lakie & Robson, 1988; see Figure 13 in Turvey & Fonseca, 2014), it is particularly prominent in the actin-myosin interactions within the muscle spindle’s intrafusal fibers (Proske,
ovements for breathing, locomotion, and feeding are critical for survival, but how they are controlled by the CNS is poorly understood. It has long been recognized that sensory information from receptors in many tissues is required for accurate movements. Such information may be transduced by receptors in the skin, joint and muscles and their associated connective tissues. Additional information about the body’s relation to the external environment derives from the vestibular apparatus, while the eye and ear provide further data. This information is considered to be compiled into a fluid functional brain map or representation of the body and its parts, a map that is consulted to plan and execute movements. Multisensory inputs and planning are also involved in the deceptively simple task of standing (e.g., Loram, Magnaaris, & Lakie, 2005). In their special review, Turvey and Fonseca (2014) tackle the medium of haptic perception on a broad dimensional scale, from subcellar components to the whole organism. They go on to propose that tensigrity, a fundamental structural property based on efficient deployment of tension and compression elements, is a unifying concept, again over a broad scale of size. The review by Turvey and Fonseca (2014) performs the helpful task of suggesting some much-needed linkages across different fields, from structural biology to neuroscience. Not surprisingly, the attempt is fraught with dangers but nonetheless it raises some important questions. I consider briefly some of the linkages and some of the controversies.
Downloaded by [Universite Laval] at 09:06 26 June 2014
M
Some Peripheral Issues An important emphasis is the functional relation between the micro and macro properties of the musculoskeletal system, and perhaps, the authors would argue, even the body as a whole. For example, it is good to be reminded that the basic mechanism of hearing should not be viewed solely in a narrow focus from the molecular behavior of the cochlear inner hair cells to the properties of the cochlear nerve fibers and then their central projections. Instead, it is better, at a more ecological level (e.g., Dusenbery, 1992) to consider the properties of the tissues in which the hair cells are embedded from the basilar membrane, back through the bones of the middle ear and the muscles which dampen their effects, to the pinna and ultimately the types of environmental vibration that are being transduced. Of course this concept can be extended to the main classes of proprioceptors. Here the muscle spindle offers some insight. This structure resides within mammalian muscles and has seemingly complex afferent and efferent connections with the central nervous system. It is well known that primary and secondary muscle spindle endings encode
Correspondence address: Simon C. Gandevia, Neuroscience Research Australia, Barker Street, Randwick, Sydney NSW 2031, Australia. e-mail: [email protected] 199
Downloaded by [Universite Laval] at 09:06 26 June 2014
S. C. Gandevia
Morgan, & Gregory, 1993). Hence, the fusimotor drive to these fibers that accompanies voluntary activity combined with changes in length of the muscle can leave its muscle spindles in a tight or more loose configuration, despite the muscle-tendon unit staying at the same length. Spindle firing is high under the tight condition and low or absent under the loose condition. This alters proprioception as the muscle will be perceived as long or short depending on the firing rate of its spindles, and it will affect the sensory response of the muscle to perturbations and hence its reflex and volitional output (for a review, see Proske & Gandevia, 2012). Intrafusal thixotropy and the variability in the response of human muscle spindles from the same muscle to a similar length change raises difficulty for the claim that the MCS should be considered a homogenous isotropic medium. The various pathways for force transfer within and between muscles and other structures (i.e., intramuscular, intermuscular, and extramuscular force transmission) are contentious. However, since the pioneering work of Street (1983) on frog muscle and subsequently by Huijing (2003, 2009; for references, see Turvey & Fonseca, 2014) on different mammalian preparations, there can be no doubt of their existence. What remains is to quantify the size of the effects and the circumstances under which they occur. At least for the human triceps surae, with the common insertion of the gastrocnemii and soleus into the Achilles tendon, there is no argument about the presence of intermuscular force transmission between medial gastrocnemius and soleus, but the available evidence suggests that the magnitude of the effect would not produce a big change in the passive length-tension curve of the ankle plantarflexors (Tian, Herbert, Hoang, Gandevia, & Bilston, 2012). In the human upper limb, there are dramatic examples of effective disconnection of muscles from their insertions on the distal phalanx depending on the length of their nearby neighbors (for details, see Van Duinen & Gandevia, 2011) such that the active contraction of flexor digitorum profundus to one finger can generate no force at its insertion. It is an example of “no force” transmission and a dramatic demonstration of the importance of the MCS for movement. However, for the long finger flexors and extensors operating within their common length ranges, the forces produced by their single motor units do not spillover to generate much force via neighboring tendons (for references, see Van Duinen & Gandevia, 2011). This provides some simplification at the level of the periphery for selective force control in the fingers. However, we are only just beginning to tackle some of deeper issues of movement control that are engendered by a realization that there is a spectrum of degrees of nonlinear force transmission. Some Central Issues If we accept that the central nervous system has to integrate the neural signals it receives to control movement, both moment-to-moment as well as over short and long time scales (e.g., for learning a skill, for adapting to limb growth), 200
then how is this achieved? This proposition is not necessarily accepted by the authors, and some theoretical limits to the coding are raised. My response is that the brain has evolved methods that do solve the coding complexity for haptic and proprioceptive perception. Thus, the brain can generate a range of possible scenarios and test them for consistency against available sensory information. This scenario-based testing model explains many proprioceptive and visual illusions (e.g., Gregory, 2009). Hence, artificially increased firing of muscle spindles (produced by vibratory or electrical stimulation of say elbow flexors) can produce a sense that the elbow joint is moving into extension, and that it occupies a more extended position, and that the body part that the hand is holding (say the nose) is lengthened. Presumably comparable solutions are available centrally for stimuli, which do not necessarily reach perception (e.g., Luu et al., 2012). An issue that has been central to many motor control theories since the time of Helmholtz, namely the differentiation of stimuli that are self-generated from those generated by the external environment, was not included in the analysis by Turvey and Fonseca of haptic perception. Clearly, a scenariobased model, or a prediction-based model, of which many have been described is required (e.g., Bays & Wolpert, 2007; Proske & Gandevia, 2012). The variety of ways in which such models need to operate has recently been described for limb movements (Walsh, Taylor, & Gandevia, 2011) and also eye movements (Whitham et al., 2010). It is difficult to see how an overarching tensigrity-based view of the peripheral structures involved in production of movement (i.e., muscles) and the consequence of movement (i.e., sensory input) can explain the differentiation noted previously. Furthermore, there are major contributions from centrally- generated signals of motor command to proprioception, both for signals of limb position and movement (Gandevia, Smith, Crawford, Proske, & Taylor, 2006; Walsh, Gandevia, & Taylor, 2010) and for signals of force (e.g., Gandevia, 1987; cf. Luu, Day, Cole, & Fitzpatrick, 2011; see also Proske & Gandevia, 2012). Concluding Comment The review by Turvey and Fonseca (2014) is stronger in exposing the peripheral mechanisms that are required for haptic, kinesthetic, or proprioceptive judgments than it is in delineating the central processes that must underlie perception and action. This should remind us that for too long the physiologists, psychologists, clinicians, and others have overemphasized the apparently separate perceptual (and other) effects due to activity in one anatomical class of receptor (i.e., those in the skin, joints, or muscles) rather than the orchestrated effects that their usual combination evokes. This likely arose from the anatomists’ natural desire to subdivide musculoskeletal tissues into muscle, joint, tendon, and aponeurosis. Furthermore, we have not broken out from the Sherringtonian terminology of proprioception and its relatives (exteroception, enteroception), Bastian’s earlier but enduring versions of kinesthesis, and the simplistic clinical term joint position Journal of Motor Behavior
Proprioception, Tensegrity, and Motor Control
sense. Hopefully a better terminology will emerge, which could helpfully link with the more encompassing view of the muscle and connective tissue network. Time will tell whether this network is the ultimate medium for haptic sensation. FUNDING The author’s research is supported by the National Health and Medical Research Council (of Australia).
Downloaded by [Universite Laval] at 09:06 26 June 2014
REFERENCES Bays, P. M., & Wolpert, D. M. (2007). Computational principles of sensorimotor control that minimize uncertainty and variability. Journal of Physiology, 578, 387–396. Burke, D., Aniss, A. M., & Gandevia, S. C. (1987). In-parallel and in-series behavior of human muscle spindle endings. Journal of Neurophysiology, 58, 417–426. Dimitriou, M., & Edin, B. B. (2008). Discharges in human muscle spindle afferents during a key-pressing task. Journal of Physiology, 586, 5455–5470. Dusenbery, D. B. (1992). Sensory ecology: How organisms acquire and respond to information. New York, NY: W. H. Freeman. Gandevia, S. C. (1987). Roles for perceived motor commands in motor control. Trends in Neurosciences, 10, 81–85. Gandevia, S. C., & Burke, D. (1992). Does the nervous system depend on kinesthetic information to control natural limb movements. Behavioral Brain Sciences, 15, 614–632 and 815–819. Gandevia, S. C., Smith, J. L., Crawford, M., Proske, U., & Taylor, J. L. (2006). Motor commands contribute to human position sense. Journal of Physiology, 571, 703–710. Gregory, R. (2009). Seeing through illusions. Oxford, England: Oxford University Press. Huijing, P. A. (2003). Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exercise and Sport Sciences Reviews, 31, 167–175. Huijing, P. A. (2009). Epimuscular myofascial force transmission: A historical review and implications for new research. Journal of Biomechanics, 42, 9–21.
2014, Vol. 46, No. 3
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