Foot anatomy specialization for postural sensation and control.

Anthropological and biomechanical research suggests that the human foot evolved a unique design for propulsion and support. In theory, the arch and toes must play an important role, however, many postural studies tend to focus on the simple hinge action of the ankle joint. To investigate further the role of foot anatomy and sensorimotor control of posture, we quantified the deformation of the foot arch and studied the effects of local perturbations applied to the toes (TOE) or 1st/2nd metatarsals (MT) while standing. In sitting position, loading and lifting a 10-kg weight on the knee respectively lowered and raised the foot arch between 1 and 1.5 mm. Less than 50% of this change could be accounted for by plantar surface skin compression. During quiet standing, the foot arch probe and shin sway revealed a significant correlation, which shows that as the tibia tilts forward, the foot arch flattens and vice versa. During TOE and MT perturbations (a 2- to 6-mm upward shift of an appropriate part of the foot at 2.5 mm/s), electromyogram (EMG) measures of the tibialis anterior and gastrocnemius revealed notable changes, and the root-mean-square (RMS) variability of shin sway increased significantly, these increments being greater in the MT condition. The slow return of RMS to baseline level (>30 s) suggested that a very small perturbation changes the surface reference frame, which then takes time to reestablish. These findings show that rather than serving as a rigid base of support, the foot is compliant, in an active state, and sensitive to minute deformations. In conclusion, the architecture and physiology of the foot appear to contribute to the task of bipedal postural control with great sensitivity.

[1]  T. Mergner,et al.  Multisensory control of human upright stance , 2006, Experimental Brain Research.

[2]  M. Bove,et al.  Interaction between vision and neck proprioception in the control of stance , 2009, Neuroscience.

[3]  F Lacquaniti,et al.  A novel approach to mechanical foot stimulation during human locomotion under body weight support. , 2011, Human movement science.

[4]  A E Patla,et al.  Ankle muscle stiffness in the control of balance during quiet standing. , 2001, Journal of neurophysiology.

[5]  J. Duysens,et al.  Dynamic Control of Location-Specific Information in Tactile Cutaneous Reflexes from the Foot during Human Walking , 1997, The Journal of Neuroscience.

[6]  A. Clifford,et al.  Postural control in healthy individuals. , 2010, Clinical biomechanics.

[7]  F. Horak,et al.  Interaction of posture and conscious perception of gravitational vertical and surface horizontal , 2007, Experimental Brain Research.

[8]  Daniel E Lieberman,et al.  The coevolution of human hands and feet. , 2010, Evolution; international journal of organic evolution.

[9]  Jesper Bencke,et al.  Foot medial longitudinal-arch deformation during quiet standing and gait in subjects with medial tibial stress syndrome. , 2008, The Journal of foot and ankle surgery : official publication of the American College of Foot and Ankle Surgeons.

[10]  Gurfinkel' Vs,et al.  The contribution of foot deformation to the changes of muscular length and angle in the ankle joint during standing in man. , 1994 .

[11]  D. Burke,et al.  Reflex responses in active muscles elicited by stimulation of low-threshold afferents from the human foot. , 1992, Journal of neurophysiology.

[12]  Romeo Chua,et al.  The role of cutaneous receptors in the foot. , 2002, Advances in experimental medicine and biology.

[13]  Hicks Jh,et al.  The mechanics of the foot. I. The joints. , 1953 .

[14]  F. Lacquaniti,et al.  Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. , 2002, Journal of neurophysiology.

[15]  B. E. Maki,et al.  The role of plantar cutaneous mechanoreceptors in the control of compensatory stepping reactions evoked by unpredictable, multi-directional perturbation , 2000, Brain Research.

[16]  J. H. Hicks,et al.  The foot as a support. , 1955, Acta anatomica.

[17]  M. Tanaka,et al.  Coding of modified body schema during tool use by macaque postcentral neurones. , 1996, Neuroreport.

[18]  K. Fujiwara,et al.  Perceived Standing Position after Reduction of Foot-Pressure Sensation by Cooling the Sole , 2003, Perceptual and motor skills.

[19]  Bill Vicenzino,et al.  Arch height change during sit-to-stand: an alternative for the navicular drop test , 2008, Journal of foot and ankle research.

[20]  J P Roll,et al.  Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation , 2001, The Journal of physiology.

[21]  Raziel Riemer,et al.  The effect of plantar flexor muscle fatigue on postural control. , 2011, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[22]  P. Gatev,et al.  Feedforward ankle strategy of balance during quiet stance in adults , 1999, The Journal of physiology.

[23]  V. S. Gurfinkel,et al.  Kinesthetic reference for human orthograde posture , 1995, Neuroscience.

[24]  P. Cavanagh,et al.  Increased variability of continuous overground walking in neuropathic patients is only indirectly related to sensory loss. , 2001, Gait & posture.

[25]  W. Wright Tonic postural lean after-effects influenced by support surface stability and dynamics. , 2011, Human movement science.

[26]  V. Macefield,et al.  Evidence for strong synaptic coupling between single tactile afferents from the sole of the foot and motoneurons supplying leg muscles. , 2005, Journal of neurophysiology.

[27]  Keir Pearson,et al.  Updating neural representations of objects during walking , 2010, Annals of the New York Academy of Sciences.

[28]  R. Fitzpatrick,et al.  Stable human standing with lower‐limb muscle afferents providing the only sensory input. , 1994, The Journal of physiology.

[29]  R Johansson,et al.  Significance of pressor input from the human feet in lateral postural control. The effect of hypothermia on galvanically induced body-sway. , 1990, Acta oto-laryngologica.

[30]  Marco Schieppati,et al.  Loss of large-diameter spindle afferent fibres is not detrimental to the control of body sway during upright stance: evidence from neuropathy , 2000, Experimental Brain Research.

[31]  P. Morasso,et al.  Can muscle stiffness alone stabilize upright standing? , 1999, Journal of neurophysiology.

[32]  V T Inman,et al.  The Human Foot , 1944, Manitoba medical review.

[33]  J. H. Hicks The mechanics of the foot. IV. The action of muscles on the foot in standing. , 1956, Acta anatomica.

[34]  J. Duysens,et al.  Load-regulating mechanisms in gait and posture: comparative aspects. , 2000, Physiological reviews.

[35]  V. Gurfinkel,et al.  The contribution of foot deformation to the changes of muscular length and angle in the ankle joint during standing in man. , 1994, Physiological research.

[36]  M.R. Popovic,et al.  Neural-Mechanical Feedback Control Scheme Generates Physiological Ankle Torque Fluctuation During Quiet Stance , 2010, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[37]  V. S. Gurfinkel,et al.  Human equilibrium on unstable support: the importance of feet-support interaction , 1997, Neuroscience Letters.

[38]  Dieter Rosenbaum,et al.  Evaluation of early walking patterns from plantar pressure distribution measurements. First year results of 42 children. , 2004, Gait & posture.

[39]  T. S. Ellis,et al.  The Human Foot , 1889, Bristol Medico-Chirurgical Journal (1883).

[40]  Y. Ivanenko,et al.  Postural instability enhances motor responses to transcranial magnetic stimulation in humans , 2003, Neuroscience Letters.

[41]  Carlo J. De Luca,et al.  The role of plantar cutaneous sensation in unperturbed stance , 2004, Experimental Brain Research.

[42]  J. Tol,et al.  Medial Tibial Stress Syndrome , 2009, Sports medicine.

[43]  Ann Hallemans,et al.  Changes in foot-function parameters during the first 5 months after the onset of independent walking: a longitudinal follow-up study. , 2006, Gait & posture.

[44]  C. Bard,et al.  Gait problems in diabetic neuropathic patients. , 1996, Archives of physical medicine and rehabilitation.

[45]  Constantinos N Maganaris,et al.  The passive, human calf muscles in relation to standing: the non‐linear decrease from short range to long range stiffness , 2007, The Journal of physiology.

[46]  Vasilios Baltzopoulos,et al.  The proprioceptive and agonist roles of gastrocnemius, soleus and tibialis anterior muscles in maintaining human upright posture , 2009, The Journal of physiology.

[47]  Ian David Loram,et al.  Paradoxical muscle movement during postural control. , 2009, Medicine and science in sports and exercise.

[48]  J. H. Hicks,et al.  The mechanics of the foot. I. The joints. , 1953, Journal of anatomy.

[49]  J. Roll,et al.  The plantar sole is a ‘dynamometric map’ for human balance control , 1998, Neuroreport.

[50]  M Schieppati,et al.  Task-dependent effects evoked by foot muscle afferents on leg muscle activity in humans. , 1996, Electroencephalography and clinical neurophysiology.

[51]  D. J. Morton,et al.  METATARSUS ATAVICUS: The Identification of a Distinctive Type of Foot Disorder , 1927 .

[52]  Måns Magnusson,et al.  Significance of Pressor Input from the Human Feet in Lateral Postural Control: The Effect of Hypothermia on Galvanically Induced Body-sway , 1990 .

[53]  A. Palma,et al.  Functional anatomy and imaging of the foot. , 2001, Italian journal of anatomy and embryology = Archivio italiano di anatomia ed embriologia.

[54]  D. Winter,et al.  Biomechanical model of the human foot: kinematics and kinetics during the stance phase of walking. , 1993, Journal of biomechanics.

[55]  P. Rack,et al.  Reflex responses at the human ankle: the importance of tendon compliance. , 1983, The Journal of physiology.

[56]  Hylton B Menz,et al.  Effects of experimentally induced plantar insensitivity on forces and pressures under the foot during normal walking. , 2004, Gait & posture.

[57]  Benedikt Hallgrímsson,et al.  THE COEVOLUTION OF HUMAN HANDS AND FEET , 2010, Evolution; international journal of organic evolution.

[58]  J. F. Yang,et al.  Phase-dependent reflex reversal in human leg muscles during walking. , 1990, Journal of neurophysiology.

[59]  T. Kiemel,et al.  Identification of the plant for upright stance in humans: multiple movement patterns from a single neural strategy. , 2008, Journal of neurophysiology.

[60]  D. Bramble,et al.  Endurance running and the evolution of Homo , 2004, Nature.

[61]  A. Nardone,et al.  Early and late stretch responses of human foot muscles induced by perturbation of stance , 2004, Experimental Brain Research.

[62]  Anne Kavounoudias,et al.  Cutaneous afferents from human plantar sole contribute to body posture awareness , 2002, Neuroreport.

[63]  R. F. Ker,et al.  The spring in the arch of the human foot , 1987, Nature.

[64]  Paolo Bonato,et al.  Noise‐enhanced balance control in patients with diabetes and patients with stroke , 2006, Annals of neurology.