Object manipulation tasks comprise sequentially organized action phases that are generally delineated by distinct mechanical contact events representing task subgoals. To achieve these subgoals, the brain selects and implements action-phase controllers that use sensory predictions and afferent signals to tailor motor output in anticipation of requirements imposed by objects' physical properties.
Crucial control operations are centred on events that mark transitions between action phases. At these events, the CNS both receives and makes predictions about sensory information from multiple sources. Mismatches between predicted and actual sensory outcomes can be used to quickly and flexibly launch corrective actions as required.
Signals from tactile afferents provide rich information about both the timing and the physical nature of contact events. In addition, they encode information related to object properties, including the shape and texture of contacted surfaces and the frictional conditions between these surfaces and the skin.
A central question is how tactile afferent information is encoded and processed by the brain for the rapid detection and analysis of contact events. Recent evidence suggests that the relative timing of spikes in ensembles of tactile afferents provides such information fast enough to account for the speed with which tactile signals are used in object manipulation tasks.
Contact events in manipulation can also be represented in the visual and auditory modalities and this enables the brain to simultaneously evaluate sensory predictions in different modalities. Multimodal representations of subgoal events also provide an opportunity for the brain to learn and uphold sensorimotor correlations that can be exploited by action-phase controllers.
A current challenge is to learn how the brain implements the control operations that support object manipulations, such as processes involved in detecting sensory mismatches, triggering corrective actions, and creating, recruiting and linking different action-phase controllers during task progression. The signal processing in somatosensory pathways for dynamic context-specific decoding of tactile afferent messages needs to be better understood, as does the role of the descending control of these pathways.
During object manipulation tasks, the brain selects and implements action-phase controllers that use sensory predictions and afferent signals to tailor motor output to the physical properties of the objects involved. Analysis of signals in tactile afferent neurons and central processes in humans reveals how contact events are encoded and used to monitor and update task performance.
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Macefield, V. G. & Johansson, R. S. Control of grip force during restraint of an object held between finger and thumb: responses of muscle and joint afferents from the digits. Exp. Brain Res. 108, 172–184 (1996).
Macefield, V. G., Häger-Ross, C. & Johansson, R. S. Control of grip force during restraint of an object held between finger and thumb: responses of cutaneous afferents from the digits. Exp. Brain Res. 108, 155–171 (1996).
Häger-Ross, C. & Johansson, R. S. Non-digital afferent input in reactive control of fingertip forces during precision grip. Exp. Brain Res. 110, 131–141 (1996).
Dimitriou, M. & Edin, B. B. Discharges in human muscle receptor afferents during block grasping. J. Neurosci. 28, 12632–12642 (2008).
Johansson, R. S. & Flanagan, J. R. in The Senses: a Comprehensive Reference, Volume 6, Somatosensation (eds Gardner, E. & Kaas, J. H.) 67–86 (Academic, San Diego, 2008).
Vallbo, A. B. & Johansson, R. S. Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. Hum. Neurobiol. 3, 3–14 (1984).
Johansson, R. S., Landström, U. & Lundström, R. Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements. Brain Res. 244, 17–25 (1982).
Löfvenberg, J. & Johansson, R. S. Regional differences and interindividual variability in sensitivity to vibration in the glabrous skin of the human hand. Brain Res. 301, 65–72 (1984).
Brisben, A. J., Hsiao, S. S. & Johnson, K. O. Detection of vibration transmitted through an object grasped in the hand. J. Neurophysiol. 81, 1548–1558 (1999).
Loewenstein, W. R. & Skalak, R. Mechanical transmission in a Pacinian corpuscle. An analysis and a theory. J. Physiol. 182, 346–378 (1966).
Westling, G. & Johansson, R. S. Responses in glabrous skin mechanoreceptors during precision grip in humans. Exp. Brain Res. 66, 128–140 (1987). Impulses in single tactile afferents innervating the human fingertips were recorded from the median nerve while small test objects were lifted, held in the air and then replaced. Distinct discharges were observed at various contact events corresponding to the completion of task subgoals.
Knibestöl, M. Stimulus-response functions of slowly adapting mechanoreceptors in the human glabrous skin area. J. Physiol. 245, 63–80 (1975).
Johansson, R. S. Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. J. Physiol. 281, 101–125 (1978).
Darian-Smith, I. in Handbook of Physiology (eds, Brookhart, J. M., Mountcastle, V. B., Darian-Smith, I. & Geiger, S. R.) 739–788 (American Physiological Society, Bethesda, Maryland, 1984).
Johnson, K. O., Yoshioka, T. & Vega-Bermudez, F. Tactile functions of mechanoreceptive afferents innervating the hand. J. Clin. Neurophysiol. 17, 539–558 (2000).
Goodwin, A. W. & Wheat, H. E. Sensory signals in neural populations underlying tactile perception and manipulation. Annu. Rev. Neurosci. 27, 53–77 (2004).
Johnson, K. O. & Hsiao, S. S. Neural mechanisms of tactual form and texture perception. Annu. Rev. Neurosci. 15, 227–250 (1992).
Craig, J. C. & Rollman, G. B. Somesthesis. Annu. Rev. Psychol. 50, 305–331 (1999).
Sathian, K., Goodwin, A. W., John, K. T. & Darian-Smith, I. Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad. J. Neurosci. 9, 1273–1279 (1989).
Johansson, R. S. & Vallbo, Å. B. Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci. 6, 27–31 (1983).
Bisley, J. W., Goodwin, A. W. & Wheat, H. E. Slowly adapting type I afferents from the sides and end of the finger respond to stimuli on the center of the fingerpad. J. Neurophysiol. 84, 57–64 (2000).
Birznieks, I., Jenmalm, P., Goodwin, A. W. & Johansson, R. S. Encoding of direction of fingertip forces by human tactile afferents. J. Neurosci. 21, 8222–8237 (2001).
Jenmalm, P., Birznieks, I., Goodwin, A. W. & Johansson, R. S. Influences of object shape on responses in human tactile afferents under conditions characteristic for manipulation. Eur. J. Neurosci. 18, 164–176 (2003).
Hinton, G. E., McClelland, J. L. & Rumelhart, D. E. in Parallel Distributed processing vol. 1 (eds Rumelhart, D. E. & McClelland, J. L.) 77–109 (MIT Press, Cambridge, Massachusetts, 1986).
Eurich, C. W. & Schwegler, H. Coarse coding: calculation of the resolution achieved by a population of large receptive field neurons. Biol. Cybern. 76, 357–363 (1997).
Maeno, T. & Kobayashi, K. FE analysis of the dynamic characteristics of the human finger pad in contact with objects with/without surface roughness. Proc. 1998 Am. Soc. Mech. Eng. Int. Mech. Eng. Congress Exposition 64, 279–286 (1998).
Maeno, T., Kobayashi, K. & Yamazaki, N. Relationship between the structure of human finger tissue and the location of tactile receptors. JSME Int. J. 41, 94–100 (1998).
Serina, E. R., Mockensturm, E., Mote, C. D. Jr & Rempel, D. A structural model of the forced compression of the fingertip pulp. J. Biomech. 31, 639–646 (1998).
Srinivasan, M. A. & Dandekar, K. An investigation of the mechanics of tactile sense using two-dimensional models of the primate fingertip. J. Biomech. Eng. 118, 48–55 (1996).
Nakazawa, N., Ikeura, R. & Inooka, H. Characteristics of human fingertips in the shearing direction. Biol. Cybern. 82, 207–214 (2000).
Dandekar, K., Raju, B. I. & Srinivasan, M. A. 3-D finite-element models of human and monkey fingertips to investigate the mechanics of tactile sense. J. Biomech. Eng. 125, 682–691 (2003).
Wu, J. Z., Dong, R. G., Smutz, W. P. & Schopper, A. W. Modeling of time-dependent force response of fingertip to dynamic loading. J. Biomech. 36, 383–392 (2003).
Wu, J. Z., Welcome, D. E. & Dong, R. G. Three-dimensional finite element simulations of the mechanical response of the fingertip to static and dynamic compressions. Comput. Methods Biomech. Biomed. Eng. 9, 55–63 (2006).
Maeno, T., Kawamura, T. & Cheng, S. C. Friction estimation by pressing an elastic finger-shaped sensor against a surface. IEEE Trans. Rob. Autom. 20, 222–2228 (2004).
Flanagan, J. R., Bowman, M. C. & Johansson, R. S. Control strategies in object manipulation tasks. Curr. Opin. Neurobiol. 16, 650–659 (2006).
Prochazka, A. The fuzzy logic of visuomotor control. Can. J. Physiol. Pharmacol. 74, 456–462 (1996).
Misiaszek, J. E. Neural control of walking balance: if falling then react else continue. Exerc. Sport Sci. Rev. 34, 128–134 (2006).
Forssberg, H., Eliasson, A. C., Kinoshita, H., Johansson, R. S. & Westling, G. Development of human precision grip. I: Basic coordination of force. Exp. Brain Res. 85, 451–457 (1991).
Forssberg, H. et al. Development of human precision grip. II. Anticipatory control of isometric forces targeted for object's weight. Exp. Brain Res. 90, 393–398 (1992).
Gordon, A. M., Forssberg, H., Johansson, R. S., Eliasson, A. C. & Westling, G. Development of human precision grip. III. Integration of visual size cues during the programming of isometric forces. Exp. Brain Res. 90, 399–403 (1992).
Forssberg, H., Eliasson, A. C., Kinoshita, H., Westling, G. & Johansson, R. S. Development of human precision grip. IV. Tactile adaptation of isometric finger forces to the frictional condition. Exp. Brain Res. 104, 323–330 (1995).
Eliasson, A. C. et al. Development of human precision grip. V. Anticipatory and triggered grip actions during sudden loading. Exp. Brain Res. 106, 425–433 (1995).
Paré, M. & Dugas, C. Developmental changes in prehension during childhood. Exp. Brain Res. 125, 239–247 (1999).
Goodale, M. A. et al. Separate neural pathways for the visual analysis of object shape in perception and prehension. Curr. Biol. 4, 604–610 (1994).
Santello, M. & Soechting, J. F. Gradual molding of the hand to object contours. J. Neurophysiol. 79, 1307–1320 (1998).
Cohen, R. G. & Rosenbaum, D. A. Where grasps are made reveals how grasps are planned: generation and recall of motor plans. Exp. Brain Res. 157, 486–495 (2004).
Cuijpers, R. H., Smeets, J. B. & Brenner, E. On the relation between object shape and grasping kinematics. J. Neurophysiol. 91, 2598–2606 (2004).
Lukos, J., Ansuini, C. & Santello, M. Choice of contact points during multidigit grasping: effect of predictability of object center of mass location. J. Neurosci. 27, 3894–3903 (2007).
Pawluk, D. T. & Howe, R. D. Dynamic lumped element response of the human fingerpad. J. Biomech. Eng. 121, 178–183 (1999).
Wheat, H. E., Goodwin, A. W. & Browning, A. S. Tactile resolution: peripheral neural mechanisms underlying the human capacity to determine positions of objects contacting the fingerpad. J. Neurosci. 15, 5582–5595 (1995).
Knibestöl, M. Stimulus-response functions of rapidly adapting mechanoreceptors in human glabrous skin area. J. Physiol. 232, 427–452 (1973).
Johansson, R. S. & Vallbo, Å. B. in Sensory Functions of the Skin in Primates, With Special Reference to Man (ed. Zotterman, Y.) 171–184 (Pergamon, Oxford, 1976).
Gentilucci, M., Toni, I., Daprati, E. & Gangitano, M. Tactile input of the hand and the control of reaching to grasp movements. Exp. Brain Res. 114, 130–137 (1997).
Lackner, J. R. & DiZio, P. A. Aspects of body self-calibration. Trends Cogn. Sci. 4, 279–288 (2000).
Rao, A. K. & Gordon, A. M. Contribution of tactile information to accuracy in pointing movements. Exp. Brain Res. 138, 438–445 (2001).
Gordon, A. M. & Soechting, J. F. Use of tactile afferent information in sequential finger movements. Exp. Brain Res. 107, 281–292 (1995).
Rabin, E. & Gordon, A. M. Tactile feedback contributes to consistency of finger movements during typing. Exp. Brain Res. 155, 362–369 (2004).
Säfström, D. & Edin, B. B. Task requirements influence sensory integration during grasping in humans. Learn. Mem. 11, 356–363 (2004).
Lemon, R. N., Johansson, R. S. & Westling, G. Corticospinal control during reach, grasp and precision lift in man. J. Neurosci. 15, 6145–6156 (1995).
Schabrun, S. M., Ridding, M. C. & Miles, T. S. Role of the primary motor and sensory cortex in precision grasping: a transcranial magnetic stimulation study. Eur. J. Neurosci. 27, 750–756 (2008).
Davare, M., Andres, M., Clerget, E., Thonnard, J. L. & Olivier, E. Temporal dissociation between hand shaping and grip force scaling in the anterior intraparietal area. J. Neurosci. 27, 3974–3980 (2007).
Davare, M., Andres, M., Cosnard, G., Thonnard, J. L. & Olivier, E. Dissociating the role of ventral and dorsal premotor cortex in precision grasping. J. Neurosci. 26, 2260–2268 (2006).
Johansson, R. S. & Westling, G. Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp. Brain Res. 56, 550–564 (1984). This study demonstrated that subjects' grip forces change in parallel with load forces to overcome forces counteracting the intended manipulation, and that the balance between the grip and load forces is adapted to the friction to provide a small safety margin to prevent slips. Experiments with local anaesthesia showed that this adaptation depends on cutaneous afferent input.
Goodwin, A. W., Jenmalm, P. & Johansson, R. S. Control of grip force when tilting objects: effect of curvature of grasped surfaces and of applied tangential torque. J. Neurosci. 18, 10724–10734 (1998).
Wing, A. M. & Lederman, S. J. Anticipating load torques produced by voluntary movements. J. Exp. Psychol. Hum. Percept. Perform. 24, 1571–1581 (1998).
Johansson, R. S., Backlin, J. L. & Burstedt, M. K. O. Control of grasp stability during pronation and supination movements. Exp. Brain Res. 128, 20–30 (1999).
Flanagan, J. R. & Wing, A. M. The stability of precision grip forces during cyclic arm movements with a hand-held load. Exp. Brain Res. 105, 455–464 (1995).
Flanagan, J. R. & Tresilian, J. R. Grip load force coupling: a general control strategy for transporting objects. J. Exp. Psychol. Hum. Percept. Perform. 20, 944–957 (1994).
LaMotte, R. H. Softness discrimination with a tool. J. Neurophysiol. 83, 1777–1786 (2000).
Flanagan, J. R., Burstedt, M. K. O. & Johansson, R. S. Control of fingertip forces in multi-digit manipulation. J. Neurophysiol. 81, 1706–1717 (1999).
Santello, M. & Soechting, J. F. Force synergies for multifingered grasping. Exp. Brain Res. 133, 457–467 (2000).
Johansson, R. S. & Westling, G. Programmed and triggered actions to rapid load changes during precision grip. Exp. Brain Res. 71, 72–86 (1988).
Burstedt, M. K. O., Edin, B. B. & Johansson, R. S. Coordination of fingertip forces during human manipulation can emerge from independent neural networks controlling each engaged digit. Exp. Brain Res. 117, 67–79 (1997).
Bracewell, R. M., Wing, A. M., Soper, H. M. & Clark, K. G. Predictive and reactive co-ordination of grip and load forces in bimanual lifting in man. Eur. J. Neurosci. 18, 2396–2402 (2003).
Witney, A. G., Goodbody, S. J. & Wolpert, D. M. Predictive motor learning of temporal delays. J. Neurophysiol. 82, 2039–2048 (1999).
Gysin, P., Kaminski, T. R. & Gordon, A. M. Coordination of fingertip forces in object transport during locomotion. Exp. Brain Res. 149, 371–379 (2003).
Witney, A. G. & Wolpert, D. M. The effect of externally generated loading on predictive grip force modulation. Neurosci. Lett. 414, 10–15 (2007).
Danion, F. & Sarlegna, F. R. Can the human brain predict the consequences of arm movement corrections when transporting an object? Hints from grip force adjustments. J. Neurosci. 27, 12839–12843 (2007).
Bursztyn, L. L. & Flanagan, J. R. Sensorimotor memory of weight asymmetry in object manipulation. Exp. Brain Res. 184, 127–133 (2008).
Flanagan, J. R. & Wing, A. M. The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J. Neurosci. 17, 1519–1528 (1997). This study showed that when moving hand-held objects, people precisely modulate their grip force in anticipation of movement-dependent loads. This result provides strong evidence that the brain learns and makes use of accurate internal models of object mechanics to predict the consequences of action.
Flanagan, J. R., Vetter, P., Johansson, R. S. & Wolpert, D. M. Prediction precedes control in motor learning. Curr. Biol. 13, 146–150 (2003).
Westling, G. & Johansson, R. S. Factors influencing the force control during precision grip. Exp. Brain Res. 53, 277–284 (1984).
Jenmalm, P. & Johansson, R. S. Visual and somatosensory information about object shape control manipulative finger tip forces. J. Neurosci. 17, 4486–4499 (1997). This study showed that people can use vision to predictively adapt their fingertip forces to the angle of grasped surfaces. The results also showed that, in the absence of vision, tactile information obtained when the fingertips contact the grasped surfaces can be used to rapidly adjust fingertip forces.
Jenmalm, P., Dahlstedt, S. & Johansson, R. S. Visual and tactile information about object curvature control fingertip forces and grasp kinematics in human dexterous manipulation. J. Neurophysiol. 84, 2984–2997 (2000).
Monzée, J., Lamarre, Y. & Smith, A. M. The effects of digital anesthesia on force control using a precision grip. J. Neurophysiol. 89, 672–683 (2003).
Nowak, D. A., Glasauer, S. & Hermsdorfer, J. How predictive is grip force control in the complete absence of somatosensory feedback? Brain 127, 182–192 (2004).
Nowak, D. A. & Hermsdörfer, J. Digit cooling influences grasp efficiency during manipulative tasks. Eur. J. Appl. Physiol. 89, 127–133 (2003).
Cole, K. J., Steyers, C. M. & Graybill, E. K. The effects of graded compression of the median nerve in the carpal canal on grip force. Exp. Brain Res. 148, 150–157 (2003).
Schenker, M., Burstedt, M. K., Wiberg, M. & Johansson, R. S. Precision grip function after hand replantation and digital nerve injury. J. Plast. Reconstr. Aesthet. Surg. 59, 706–716 (2006).
Cadoret, G. & Smith, A. M. Friction, not texture, dictates grip forces used during object manipulation. J. Neurophysiol. 75, 1963–1969 (1996).
Edin, B. B., Westling, G. & Johansson, R. S. Independent control of fingertip forces at individual digits during precision lifting in humans. J. Physiol. 450, 547–564 (1992).
Birznieks, I., Burstedt, M. K. O., Edin, B. B. & Johansson, R. S. Mechanisms for force adjustments to unpredictable frictional changes at individual digits during two-fingered manipulation. J. Neurophysiol. 80, 1989–2002 (1998).
Burstedt, M. K. O., Flanagan, R. & Johansson, R. S. Control of grasp stability in humans under different frictional conditions during multi-digit manipulation. J. Neurophysiol. 82, 2393–2405 (1999).
Quaney, B. M. & Cole, K. J. Distributing vertical forces between the digits during gripping and lifting: the effects of rotating the hand versus rotating the object. Exp. Brain Res. 155, 145–155 (2004).
Niu, X., Latash, M. L. & Zatsiorsky, V. M. Prehension synergies in the grasps with complex friction patterns: local versus synergic effects and the template control. J. Neurophysiol. 98, 16–28 (2007).
Johansson, R. S. & Westling, G. Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Exp. Brain Res. 66, 141–154 (1987).
Sathian, K. Tactile sensing of surface features. Trends Neurosci. 12, 513–519 (1989).
Johansson, R. S., Landström, U. & Lundström, R. Sensitivity to edges of mechanoreceptive afferent units innervating the glabrous skin of the human head. Brain Res. 244, 27–35 (1982).
Phillips, J. R., Johansson, R. S. & Johnson, K. O. Representation of braille characters in human nerve fibres. Exp. Brain Res. 81, 589–592 (1990).
Phillips, J. R., Johansson, R. S. & Johnson, K. O. Responses of human mechanoreceptive afferents to embossed dot arrays scanned across fingerpad skin. J. Neurosci. 12, 827–839 (1992).
Goodwin, A. W., Macefield, V. G. & Bisley, J. W. Encoding of object curvature by tactile afferents from human fingers. J. Neurophysiol. 78, 2881–2888 (1997).
Khalsa, P. S., Friedman, R. M., Srinivasan, M. A. & Lamotte, R. H. Encoding of shape and orientation of objects indented into the monkey fingerpad by populations of slowly and rapidly adapting mechanoreceptors. J. Neurophysiol. 79, 3238–3251 (1998).
Johansson, R. S. & Vallbo, A. B. Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J. Physiol. 286, 283–300 (1979).
Ehrsson, H. E., Fagergren, A., Johansson, R. S. & Forssberg, H. Evidence for the involvement of the posterior parietal cortex in coordination of fingertip forces for grasp stability in manipulation. J. Neurophysiol. 90, 3295–3303 (2003).
Kawato, M. et al. Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Prog. Brain Res. 142, 171–188 (2003).
Boecker, H. et al. Force level independent representations of predictive grip force-load force coupling: a PET activation study. Neuroimage 25, 243–252 (2005).
Wolpert, D. M., Miall, C. R. & Kawato, M. Internal models in the cerebellum. Trends Cogn. Sci. 2, 338–347 (1998).
Rost, K., Nowak, D. A., Timmann, D. & Hermsdörfer, J. Preserved and impaired aspects of predictive grip force control in cerebellar patients. Clin. Neurophysiol. 116, 1405–1414 (2005).
Nowak, D. A., Hermsdörfer, J., Marquardt, C. & Fuchs, H. H. Grip and load force coupling during discrete vertical arm movements with a grasped object in cerebellar atrophy. Exp. Brain Res. 145, 28–39 (2002).
Müller, F. & Dichgans, J. Dyscoordination of pinch and lift forces during grasp in patients with cerebellar lesions. Exp. Brain Res. 101, 485–492 (1994).
Babin-Ratté, S., Sirigu, A., Gilles, M. & Wing, A. Impaired anticipatory finger grip-force adjustments in a case of cerebellar degeneration. Exp. Brain Res. 128, 81–85 (1999).
Serrien, D. J. & Wiesendanger, M. Role of the cerebellum in tuning anticipatory and reactive grip force responses. J. Cogn. Neurosci. 11, 672–681 (1999).
Fellows, S. J., Ernst, J., Schwarz, M., Töpper, R. & Noth, J. Precision grip deficits in cerebellar disorders in man. Neurophysiol. Clin. 112, 1793–1802 (2001).
Hermsdörfer, J., Hagl, E., Nowak, D. A. & Marquardt, C. Grip force control during object manipulation in cerebral stroke. Clin. Neurophysiol. 114, 915–929 (2003).
Nowak, D. A., Hermsdörfer, J. & Topka, H. Deficits of predictive grip force control during object manipulation in acute stroke. J. Neurol. 250, 850–860 (2003).
Müller, F. & Abbs, J. H. in Advances in Neurology vol. 53 (eds Streifler, M. B., Korezyn, A. D., Melamed, E. & Youdim, M. B. H.) 191–195 (Raven, New York, 1990).
Harrison, L. M., Mayston, M. J. & Johansson, R. S. Reactive control of precision grip does not depend on fast transcortical reflex pathways in X-linked Kallmann subjects. J. Physiol. 527, 641–652 (2000).
Nowak, D. A., Voss, M., Huang, Y. Z., Wolpert, D. M. & Rothwell, J. C. High-frequency repetitive transcranial magnetic stimulation over the hand area of the primary motor cortex disturbs predictive grip force scaling. Eur. J. Neurosci. 22, 2392–2396 (2005).
Berner, J., Schönfeldt-Lecuona, C. & Nowak, D. A. Sensorimotor memory for fingertip forces during object lifting: the role of the primary motor cortex. Neuropsychologia 45, 1931–1938 (2007).
Nowak, D. A., Hermsdörfer, J. & Topka, H. When motor execution is selectively impaired: control of manipulative finger forces in amyotrophic lateral sclerosis. Motor Control 7, 304–320 (2003).
Gordon, A. M., Quinn, L., Reilmann, R. & Marder, K. Coordination of prehensile forces during precision grip in Huntington's disease. Exp. Neurol. 163, 136–148 (2000).
Serrien, D. J., Burgunder, J. M. & Wiesendanger, M. Grip force scaling and sequencing of events during a manipulative task in Huntington's disease. Neuropsychologia 39, 734–741 (2001).
Fellows, S. J., Noth, J. & Schwarz, M. Precision grip and Parkinson's disease. Brain 121, 1771–1784 (1998).
Serrien, D. J., Burgunder, J. M. & Wiesendanger, M. Disturbed sensorimotor processing during control of precision grip in patients with writer's cramp. Mov. Disord. 15, 965–972 (2000).
Schenk, T. & Mai, N. Is writer's cramp caused by a deficit of sensorimotor integration? Exp. Brain Res. 136, 321–330 (2001).
Wiesendanger, M. & Serrien, D. J. Neurological problems affecting hand dexterity. Brain Res. Brain Res. Rev. 36, 161–168 (2001).
Johansson, R. S. & Westling, G. Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Exp. Brain Res. 71, 59–71 (1988).
Gordon, A. M., Forssberg, H., Johansson, R. S. & Westling, G. Integration of sensory information during the programming of precision grip: comments on the contributions of size cues. Exp. Brain Res. 85, 226–229 (1991).
Gordon, A. M., Westling, G., Cole, K. J. & Johansson, R. S. Memory representations underlying motor commands used during manipulation of common and novel objects. J. Neurophysiol. 69, 1789–1796 (1993). The authors showed that humans use anticipatory control to scale motor commands to the weight of familiar objects. The memory information is robust and can be retrieved through visual identification of the target object. In addition, accurate memory representations related to the weights of novel objects develop quickly.
Flanagan, J. R. & Beltzner, M. A. Independence of perceptual and sensorimotor predictions in the size–weight illusion. Nature Neurosci. 3, 737–741 (2000).
Flanagan, J. R., Bittner, J. P. & Johansson, R. S. Experience can change distinct size-weight priors engaged in lifting objects and judging their weights. Curr. Biol. 18, 1742–1747 (2008). This paper showed that the motor and perceptual systems rely on distinct learned size–weight maps when lifting objects and judging their weights, respectively, and that these maps can be changed by experience.
Cole, K. J. Lifting a familiar object: visual size analysis, not memory for object weight, scales lift force. Exp. Brain Res. 188, 551–557 (2008).
Cole, K. J. & Rotella, D. L. Old age impairs the use of arbitrary visual cues for predictive control of fingertip forces during grasp. Exp. Brain Res. 143, 35–41 (2002).
Ameli, M., Dafotakis, M., Fink, G. R. & Nowak, D. A. Predictive force programming in the grip-lift task: the role of memory links between arbitrary cues and object weight. Neuropsychologia 46, 2383–2388 (2008).
Salimi, I., Hollender, I., Frazier, W. & Gordon, A. M. Specificity of internal representations underlying grasping. J. Neurophysiol. 84, 2390–2397 (2000).
Salimi, I., Frazier, W., Reilmann, R. & Gordon, A. M. Selective use of visual information signaling objects' center of mass for anticipatory control of manipulative fingertip forces. Exp. Brain Res. 150, 9–18 (2003).
Jenmalm, P., Schmitz, C., Forssberg, H. & Ehrsson, H. H. Lighter or heavier than predicted: neural correlates of corrective mechanisms during erroneously programmed lifts. J. Neurosci. 26, 9015–9021 (2006). This study examined central contributions to precision lifting using fMRI. The results suggested a role for the right inferior parietal cortex in detecting mismatches between predicted and actual weight and indicated that the primary sensorimotor cortex and the cerebellum are engaged in implementing corrective action programmes.
Desmurget, M. et al. Role of the posterior parietal cortex in updating reaching movements to a visual target. Nature Neurosci. 2, 563–567 (1999).
Tunik, E., Frey, S. H. & Grafton, S. T. Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp. Nature Neurosci. 8, 505–511 (2005).
Bursztyn, L. L., Ganesh, G., Imamizu, H., Kawato, M. & Flanagan, J. R. Neural correlates of internal-model loading. Curr. Biol. 16, 2440–2445 (2006).
Hua, S. E. & Houk, J. C. Cerebellar guidance of premotor network development and sensorimotor learning. Learn. Mem. 4, 63–76 (1997).
Chouinard, P. A., Leonard, G. & Paus, T. Role of the primary motor and dorsal premotor cortices in the anticipation of forces during object lifting. J. Neurosci. 25, 2277–2284 (2005). This paper showed that repetitive TMS applied to the dorsal premotor cortex disrupts associative memory for weight whereas repetitive TMS applied to the primary motor cortex disrupts sensorimotor memory for weight.
Li, Y., Randerath, J., Goldenberg, G. & Hermsdörfer, J. Grip forces isolated from knowledge about object properties following a left parietal lesion. Neurosci. Lett. 426, 187–191 (2007).
Adrian, E. D. The Basis of Sensation (Norton, New York, 1928).
Torebjörk, H. E., Vallbo, A. B. & Ochoa, J. L. Intraneural microstimulation in man. Its relation to specificity of tactile sensations. Brain 110, 1509–1529 (1987).
Johansson, R. S. & Birznieks, I. First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nature Neurosci. 7, 170–177 (2004). This study demonstrated that the relative timing of first impulses elicited in ensembles of tactile afferents when fingertips contact objects conveys information about the direction of fingertip forces and surface shape faster than the fastest possible rate code and fast enough to account for the use of this information in natural manipulations.
Johansson, R. S. & Vallbo, A. B. Spatial properties of the population of mechanoreceptive units in the glabrous skin of the human hand. Brain Res. 184, 353–366 (1980).
Heil, P. First-spike latency of auditory neurons revisited. Curr. Opin. Neurobiol. 14, 461–467 (2004).
VanRullen, R., Guyonneau, R. & Thorpe, S. J. Spike times make sense. Trends Neurosci. 28, 1–4 (2005).
Furukawa, S., Xu, L. & Middlebrooks, J. C. Coding of sound-source location by ensembles of cortical neurons. J. Neurosci. 20, 1216–1228 (2000).
Nelken, I., Chechik, G., Mrsic-Flogel, T. D., King, A. J. & Schnupp, J. W. Encoding stimulus information by spike numbers and mean response time in primary auditory cortex. J. Comput. Neurosci. 19, 199–221 (2005).
Reich, D. S., Mechler, F. & Victor, J. D. Temporal coding of contrast in primary visual cortex: when, what, and why. J. Neurophysiol. 85, 1039–1050 (2001).
Gawne, T. J., Kjaer, T. W. & Richmond, B. J. Latency: another potential code for feature binding in striate cortex. J. Neurophysiol. 76, 1356–1360 (1996).
Gollisch, T. & Meister, M. Rapid neural coding in the retina with relative spike latencies. Science 319, 1108–1111 (2008). The authors reported that retinal ganglion cells can encode the spatial structure of a briefly presented image in the relative timing of their first spikes. This mechanism allows the retina to rapidly and reliably transmit new spatial information with the very first spikes emitted by a neural population in a manner that is largely unaffected by stimulus contrast.
Panzeri, S., Petersen, R. S., Schultz, S. R., Lebedev, M. & Diamond, M. E. The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29, 769–777 (2001).
Petersen, R. S., Panzeri, S. & Diamond, M. E. Population coding in somatosensory cortex. Curr. Opin. Neurobiol. 12, 441–447 (2002).
Mikula, S. & Niebur, E. Rate and synchrony in feedforward networks of coincidence detectors: analytical solution. Neural Comput. 17, 881–902 (2005).
Gerstner, W. & Kistler, W. M. Spiking Neuron Models (Cambridge Univ. Press, Cambridge, 2002).
Hopfield, J. J. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33–36 (1995).
König, P., Engel, A. K. & Singer, W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130–137 (1996).
Masquelier, T., Guyonneau, R. & Thorpe, S. J. Spike timing dependent plasticity finds the start of repeating patterns in continuous spike trains. PLoS ONE 3, e1377 (2008).
Markram, H., Lübke, J., Frotscher, M. & Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213–215 (1997).
Bi, G. & Poo, M. Distributed synaptic modification in neural networks induced by patterned stimulation. Nature 401, 792–796 (1999).
Song, S., Miller, K. D. & Abbott, L. F. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nature Neurosci. 3, 919–926 (2000).
Fox, K. & Wong, R. O. A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48, 465–477 (2005).
Guyonneau, R., VanRullen, R. & Thorpe, S. J. Neurons tune to the earliest spikes through STDP. Neural Comput. 17, 859–879 (2005).
Gütig, R. & Sompolinsky, H. The tempotron: a neuron that learns spike timing-based decisions. Nature Neurosci. 9, 420–428 (2006).
Chase, S. M. & Young, E. D. First-spike latency information in single neurons increases when referenced to population onset. Proc. Natl Acad. Sci. USA 104, 5175–5180 (2007).
Jones, E. G. Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annu. Rev. Neurosci. 23, 1–37 (2000).
Kakuda, N. Conduction velocity of low-threshold mechanoreceptive afferent fibers in the glabrous and hairy skin of human hands measured with microneurography and spike-triggered averaging. Neurosci. Res. 15, 179–188 (1992).
Darian-Smith, I. & Kenins, P. Innervation density of mechanoreceptive fibres supplying glabrous skin of the monkey's index finger. J. Physiol. 309, 147–155 (1980).
Carr, C. E. Processing of temporal information in the brain. Annu. Rev. Neurosci. 16, 223–243 (1993).
Land, M. F. & Furneaux, S. The knowledge base of the oculomotor system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 1231–1239 (1997).
Flanagan, J. R. & Johansson, R. S. Action plans used in action observation. Nature 424, 769–771 (2003).
Ballard, D. H., Hayhoe, M. M., Li, F. & Whitehead, S. D. Hand-eye coordination during sequential tasks. Philos. Trans. R. Soc. Lond. B Biol. Sci. 337, 331–338 (1992).
Land, M., Mennie, N. & Rusted, J. The roles of vision and eye movements in the control of activities of daily living. Perception 28, 1311–1328 (1999).
Johansson, R. S., Westling, G., Bäckström, A. & Flanagan, J. R. Eye-hand coordination in object manipulation. J. Neurosci. 21, 6917–6932 (2001). This study examined the precise spatial and temporal coordination of gaze and fingertip movements in an object manipulation task. The results showed that the gaze supports hand movement planning by marking key positions to which the fingertips or the grasped object are subsequently directed.
Biguer, B., Jeannerod, M. & Prablanc, C. The coordination of eye, head, and arm movements during reaching at a single visual target. Exp. Brain Res. 46, 301–304 (1982).
Sailer, U., Flanagan, J. R. & Johansson, R. S. Eye–hand coordination during learning of a novel visuomotor task. J. Neurosci. 25, 8833–8842 (2005). This study examined changes in gaze behaviour during a visuomotor task in which subjects gradually learned a novel mapping between their hand actions and the movements of a cursor that they were required to move to targets. During learning, gaze behaviour shifted from a reactive mode, in which the gaze chased the cursor, to a predictive mode in which the gaze led the cursor to the targets.
Prablanc, C., Desmurget, M. & Gréa, H. Neural control of on-line guidance of hand reaching movements. Prog. Brain Res. 142, 155–170 (2003).
Paillard, J. Fast and slow feedback loops for the visual correction of spatial errors in a pointing task: a reappraisal. Can. J. Physiol. Pharmacol. 74, 401–417 (1996).
Saunders, J. A. & Knill, D. C. Visual feedback control of hand movements. J. Neurosci. 24, 3223–3234 (2004).
Sarlegna, F. et al. Online control of the direction of rapid reaching movements. Exp. Brain Res. 157, 468–471 (2004).
Downar, J., Crawley, A. P., Mikulis, D. J. & Davis, K. D. A multimodal cortical network for the detection of changes in the sensory environment. Nature Neurosci. 3, 277–283 (2000).
Bremmer, F. et al. Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29, 287–296 (2001).
Beauchamp, M. S., Yasar, N. E., Frye, R. E. & Ro, T. Touch, sound and vision in human superior temporal sulcus. Neuroimage 41, 1011–1020 (2008).
Avillac, M., Ben Hamed, S. & Duhamel, J. R. Multisensory integration in the ventral intraparietal area of the macaque monkey. J. Neurosci. 27, 1922–1932 (2007).
Schroeder, C. E. & Foxe, J. J. The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. Brain Res. Cogn. Brain Res. 14, 187–198 (2002).
Miall, R. C. & Wolpert, D. M. Forward models for physiological motor control. Neural Netw. 9, 1265–1279 (1996).
Wolpert, D. M. & Ghahramani, Z. Computational principles of movement neuroscience. Nature Neurosci. 3 (Suppl.), 1212–1217 (2000).
Wolpert, D. M. & Flanagan, J. R. Motor prediction. Curr. Biol. 11, R729–R732 (2001).
Todorov, E. & Jordan, M. I. Optimal feedback control as a theory of motor coordination. Nature Neurosci. 5, 1226–1235 (2002).
Scott, S. H. Optimal feedback control and the neural basis of volitional motor control. Nature Rev. Neurosci. 5, 532–546 (2004).
Liu, D. & Todorov, E. Evidence for the flexible sensorimotor strategies predicted by optimal feedback control. J. Neurosci. 27, 9354–9368 (2007).
Olivier, E., Davare, M., Andres, M. & Fadiga, L. Precision grasping in humans: from motor control to cognition. Curr. Opin. Neurobiol. 17, 644–648 (2007).
Mussa-Ivaldi, F. A. & Bizzi, E. Motor learning through the combination of primitives. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1755–1769 (2000).
Graziano, M. S. & Aflalo, T. N. Mapping behavioral repertoire onto the cortex. Neuron 56, 239–251 (2007).
Flash, T. & Hochner, B. Motor primitives in vertebrates and invertebrates. Curr. Opin. Neurobiol. 15, 660–666 (2005).
Stephan, K. E. et al. Nonlinear dynamic causal models for fMRI. Neuroimage 42, 649–662 (2008).
Averbeck, B. B., Chafee, M. V., Crowe, D. A. & Georgopoulos, A. P. Parallel processing of serial movements in prefrontal cortex. Proc. Natl Acad. Sci. USA 99, 13172–13177 (2002).
Saito, N., Mushiake, H., Sakamoto, K., Itoyama, Y. & Tanji, J. Representation of immediate and final behavioral goals in the monkey prefrontal cortex during an instructed delay period. Cereb. Cortex 15, 1535–1546 (2005).
Tanji, J. & Hoshi, E. Role of the lateral prefrontal cortex in executive behavioral control. Physiol. Rev. 88, 37–57 (2008).
Obhi, S. S. Bimanual coordination: an unbalanced field of research. Motor Control 8, 111–120 (2004).
Swinnen, S. P. & Wenderoth, N. Two hands, one brain: cognitive neuroscience of bimanual skill. Trends Cogn. Sci. 8, 18–25 (2004).
Ivry, R. B., Diedrichsen, J., Spencer, R. C. M., Hazeltine, E. & Semjen, A. in Neuro-behavioral Determinants of Interlimb Coordination (eds Swinnen, S. & Duysens, J.) 259–295 (Kluwer, Boston, 2004).
Johansson, R. S. et al. How a lateralized brain supports symmetrical bimanual tasks. PLoS Biol. 4, 1025–1034 (2006).
Theorin, A. & Johansson, R. S. Zones of bimanual and unimanual preference within human primary sensorimotor cortex during object manipulation. Neuroimage 36 (Suppl. 2), T2–T15 (2007).
Pubols, B. H. Jr. Factors affecting cutaneous mechanoreceptor response. II. Changes in mechanical properties of skin with repeated stimulation. J. Neurophysiol. 47, 530–542 (1982).
Harris, F., Jabbur, S. J., Morse, R. W. & Towe, A. L. Influence of the cerebral cortex on the cuneate nucleus of the monkey. Nature 208, 1215–1216 (1965).
Adkins, R. J., Morse, R. W. & Towe, A. L. Control of somatosensory input by cerebral cortex. Science 153, 1020–1022 (1966).
Ergenzinger, E. R., Glasier, M. M., Hahm, J. O. & Pons, T. P. Cortically induced thalamic plasticity in the primate somatosensory system. Nature Neurosci. 1, 226–229 (1998).
Palmeri, A., Bellomo, M., Giuffrida, R. & Sapienza, S. Motor cortex modulation of exteroceptive information at bulbar and thalamic lemniscal relays in the cat. Neuroscience 88, 135–150 (1999).
Seki, K., Perlmutter, S. I. & Fetz, E. E. Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nature Neurosci. 6, 1309–1316 (2003). The authors reported evidence from behaving monkeys that presynaptic inhibition produced by central commands in descending pathways during wrist movements effectively modulates cutaneous inputs to the spinal cord in a behaviour-dependent manner by reducing synaptic transmission at the initial synapse.
Canedo, A. Primary motor cortex influences on the descending and ascending systems. Prog. Neurobiol. 51, 287–335 (1997).
Crapse, T. B. & Sommer, M. A. Corollary discharge circuits in the primate brain. Curr. Opin. Neurobiol. 1 Nov 2008 (doi:10.1016/j.conb.2008.09.017).
Poulet, J. F. & Hedwig, B. New insights into corollary discharges mediated by identified neural pathways. Trends Neurosci. 30, 14–21 (2007).
von Holst, E. Relations between the central nervous system and the peripheral organ. Br. J. Anim. Behav. 2, 89–94 (1954).
Boyd, I. A. & Roberts, T. D. Proprioceptive discharges from stretch-receptors in the knee-joint of the cat. J. Physiol. 122, 38–58 (1953).
Gelfan, S. & Carter, S. Muscle sense in man. Exp. Neurol. 18, 469–473 (1967).
Goodwin, G. M., McCloskey, D. I. & Matthews, P. B. The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 95, 705–748 (1972).
Matthews, P. B. C. Where does Sherrington's “muscular sense” originate? Muscles, joints, corollary discharges? Annu. Rev. Neurosci. 5, 189–218 (1982).
Johansson, R. S., Trulsson, M., Olsson, K. A. & Abbs, J. H. Mechanoreceptive afferent activity in the infraorbital nerve in man during speech and chewing movements. Exp. Brain Res. 72, 209–214 (1988).
Edin, B. B. & Abbs, J. H. Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. J. Neurophysiol. 65, 657–670 (1991).
Edin, B. B. Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. J. Neurophysiol. 67, 1105–1113 (1992).
Grill, S. E. & Hallett, M. Velocity sensitivity of human muscle spindle afferents and slowly adapting type II cutaneous mechanoreceptors. J. Physiol. 489, 593–602 (1995).
Edin, B. B. Quantitative analyses of dynamic strain sensitivity in human skin mechanoreceptors. J. Neurophysiol. 92, 3233–3243 (2004).
Edin, B. Cutaneous afferents provide information about knee joint movements in humans. J. Physiol. 531, 289–297 (2001).
Aimonetti, J. M., Hospod, V., Roll, J. P. & Ribot-Ciscar, E. Cutaneous afferents provide a neuronal population vector that encodes the orientation of human ankle movements. J. Physiol. 580, 649–658 (2007).
Edin, B. B. & Johansson, N. Skin strain patterns provide kinaesthetic information to the human central nervous system. J. Physiol. 487, 243–251 (1995).
Collins, D. F. & Prochazka, A. Movement illusions evoked by ensemble cutaneous input from the dorsum of the human hand. J. Physiol. 496, 857–871 (1996).
Collins, D. F., Refshauge, K. M. & Gandevia, S. C. Sensory integration in the perception of movements at the human metacarpophalangeal joint. J. Physiol. 529, 505–515 (2000).
Collins, D. F., Refshauge, K. M., Todd, G. & Gandevia, S. C. Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J. Neurophysiol. 94, 1699–1706 (2005).
Johansson, R. S. & Edin, B. B. Predictive feed-forward sensory control during grasping and manipulation in man. Biomed. Res. 14, 95–106 (1993).
Johansson, R. S. & Cole, K. J. Sensory-motor coordination during grasping and manipulative actions. Curr. Opin. Neurobiol. 2, 815–823 (1992).
The Swedish Research Council (project 08667), the sixth Framework Program of the EU (project IST-028056), and the Canadian Institutes of Health Research supported this work.
- Tactile afferents
Fast-conducting myelinated afferent neurons that convey signals to the brain from low-threshold mechanoreceptors in body areas that actively contact objects — that is, the inside of the hand, the sole of the foot, the lips, the tongue and the oral mucosa.
- Proprioceptive afferents
Fast-conducting myelinated afferents that provide information about joint configurations and muscle states. These include mechanoreceptive afferents from the hairy skin, muscles, joints and connective tissues.
- Action-phase controller
A learned sensorimotor 'control policy' that uses specific sensory information and sensory predictions to generate motor commands to attain a sensory goal.
- Sensorimotor control point
A planned contact event in which predicted and actual sensory signals are compared to assess the outcome of an executed action-phase controller.
- Transcranial magnetic stimulation
(TMS). A non-invasive technique that can be used to induce a transient interruption of normal activity in a restricted area of the brain. It is based on the generation of a magnetic pulse near the area of interest that induces small eddy currents that stimulate neurons.
- Grasp stability
The control of grip forces such that they are adequate to prevent accidental slips but not so large that they cause unnecessary fatigue or damage to the object or hand.
- Forward internal models
Neural circuits that mimic the behaviour of the motor system and environment and capture the mapping between motor commands and expected sensory consequences.
- Corollary discharge
An internal signal, derived in part from motor commands, that can be used to estimate the time-varying afferent input that corresponds to the predicted sensory consequences of the motor command.
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Johansson, R., Flanagan, J. Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat Rev Neurosci 10, 345–359 (2009). https://doi.org/10.1038/nrn2621
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