Interaction of pre‐programmed control and natural stretch reflexes in human landing movements

Pre‐programmed mechanisms of motor control are known to influence the gain of artificially evoked stretch reflexes. However, their interaction with stretch reflexes evoked in the context of unimpeded natural movement is not understood. We used a landing movement, for which a stretch reflex is an integral part of the natural action, to test the hypothesis that unpredicted motor events increase stretch reflex gain. The unpredicted event occurred when a false floor, perceived to be solid, collapsed easily on impact, allowing the subjects to descend for a further 85 ms to a solid floor below. Spinal stretch reflexes were measured following solid floor contact. When subjects passed through the false floor en route to the solid floor, the amplitude of the EMG reflex activity was double that found in direct falls. This was not due to differences in joint rotations between these conditions. Descending pathways can modify H‐ and stretch‐reflex gain in man. We therefore manipulated the time between the false and real floor contacts and hence the time available for transmission along these pathways. With 30 ms between floors, the enhancement of the reflex was extinguished, whereas with 50 ms between floors it reappeared. This excluded several mechanisms from being responsible for the doubling of the reflex EMG amplitude. It is argued that the enhanced response is due to the modulation of reflex gain at the spinal level by signals in descending pathways triggered by the false platform. The results suggest the future hypothesis that this trigger could be the absence of afferent signals expected at the time of false floor impact and that salient error signals produced from a comparison of expected and actual sensory events may be used to reset reflex gains.

[1]  D. Burke,et al.  Changes in presynaptic inhibition of afferents to propriospinal‐like neurones in man during voluntary contractions. , 1992, The Journal of physiology.

[2]  A Schmied,et al.  Mechanical cutaneous stimulation alters Ia presynaptic inhibition in human wrist extensor muscles: a single motor unit study , 2000, The Journal of physiology.

[3]  M J McDonagh,et al.  Stretch reflex distinguished from pre‐programmed muscle activations following landing impacts in man , 2000, The Journal of physiology.

[4]  K. J. Cole,et al.  Sensory-motor coordination during grasping and manipulative actions , 1992, Current Opinion in Neurobiology.

[5]  R S Johansson,et al.  Sensory input and control of grip. , 1998, Novartis Foundation symposium.

[6]  M. F. Reschke,et al.  Vestibulo-spinal response modification as determined with the H-reflex during the Spacelab-1 flight , 2004, Experimental Brain Research.

[7]  W. Barnes Propioceptive influences on motor output during walking in the crayfish. , 1977, Journal de physiologie.

[8]  R Greenwood,et al.  Landing from an unexpected fall and a voluntary step. , 1976, Brain : a journal of neurology.

[9]  J. Nielsen,et al.  Central facilitation of Ia inhibition during tonic ankle dorsiflexion revealed after blockade of peripheral feedback , 2004, Experimental Brain Research.

[10]  J H Challis,et al.  Visual and non‐visual control of landing movements in humans , 2001, The Journal of physiology.

[11]  V. Dietz,et al.  SIGNIFICANCE OF SPINAL STRETCH REFLEXES IN HUMAN LOCOMOTION , 1981 .

[12]  S. Grillner Locomotion in vertebrates: central mechanisms and reflex interaction. , 1975, Physiological reviews.

[13]  J. Iles,et al.  Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb. , 1996, The Journal of physiology.

[14]  D. Burke,et al.  Mental rehearsal of motor tasks recruits α‐motoneurones but fails to recruit human fusimotor neurones selectively , 1997, The Journal of physiology.

[15]  K. J. Cole,et al.  Sensory-motor coordination during grasping and manipulative actions , 1992, Current Biology.

[16]  K. Pearson,et al.  Corrective responses to loss of ground support during walking. II. Comparison of intact and chronic spinal cats. , 1994, Journal of neurophysiology.

[17]  M Santello,et al.  The control of timing and amplitude of EMG activity in landing movements in humans , 1998, Experimental physiology.

[18]  Barnes Wj Propioceptive influences on motor output during walking in the crayfish. , 1977 .

[19]  A Thorstensson,et al.  Differences in modulation of the gastrocnemius and soleus H-reflexes during hopping in man. , 1990, Acta Physiologica Scandinavica.

[20]  A M Bronstein,et al.  EMG-responses to sudden onset free fall. , 1995, Acta oto-laryngologica. Supplementum.

[21]  J. D. Coulter,et al.  Sensory transmission through lemniscal pathway during voluntary movement in the cat. , 1974, Journal of neurophysiology.

[22]  Rn Lemon Sensory gating during movement: how and why? , 1997 .

[23]  H. Hultborn State‐dependent modulation of sensory feedback , 2001, The Journal of physiology.

[24]  J. Duysens,et al.  Selective activation of human soleus or gastrocnemius in reflex responses during walking and running , 2004, Experimental Brain Research.

[25]  E. Zehr,et al.  What functions do reflexes serve during human locomotion? , 1999, Progress in Neurobiology.

[26]  E. Holst Relations between the central Nervous System and the peripheral organs , 1954 .

[27]  Tamar Flash,et al.  Computational approaches to motor control , 2001, Current Opinion in Neurobiology.

[28]  A. Prochazka Sensorimotor gain control: A basic strategy of motor systems? , 1989, Progress in Neurobiology.