Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli

Zill SN, Dallmann CJ, Büschges A, Chaudhry S, Schmitz J (2018)
Journal of Neurophysiology 120(4): 1807-1823.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Zill, Sasha N.; Dallmann, Chris J.; Büschges, Ansgar; Chaudhry, Sumaiya; Schmitz, JosefUniBi
Abstract / Bemerkung
Many sensory systems are tuned to specific parameters of behaviors and have effects that are task-specific. We have studied how force feedback contributes to activation of synergist muscles in serially homologous legs of stick insects. Forces were applied using conventional half sine or ramp and hold functions. We also utilized waveforms of joint torques calculated from experiments in freely walking animals. In all legs, forces applied to either the tarsus (foot) or proximal leg segment (trochanter) activated synergist muscles that generate substrate grip and support but coupling of the depressor muscle to tarsal forces was weak in the front legs. Activation of trochanteral receptors using ramp and hold functions generated positive feedback to the depressor muscle in all legs when animals were induced to seek substrate grip. However, discharges of the synergist flexor muscle showed adaptation at moderate force levels. In contrast, application of forces using torque waveforms, which do not have a static hold phase, produced sustained discharges in muscle synergies with little adaptation. Firing frequencies reflected the magnitude of ground reaction forces, were graded to changes in force amplitude and could also be modulated by transient force perturbations added to the waveforms. Comparison of synergist activation by torques and ramp and hold functions revealed a strong influence of force dynamics (dF/dt). These studies support the idea that force receptors can act to synchronously tune muscle synergies to the range of force magnitudes and dynamics that occur in each leg according to their specific use in behaviorMany sensory systems are tuned to specific parameters of behaviors and have effects that are task-specific. We have studied how force feedback contributes to activation of synergist muscles in serially homologous legs of stick insects. Forces were applied using conventional half sine or ramp and hold functions. We also utilized waveforms of joint torques calculated from experiments in freely walking animals. In all legs, forces applied to either the tarsus (foot) or proximal leg segment (trochanter) activated synergist muscles that generate substrate grip and support but coupling of the depressor muscle to tarsal forces was weak in the front legs. Activation of trochanteral receptors using ramp and hold functions generated positive feedback to the depressor muscle in all legs when animals were induced to seek substrate grip. However, discharges of the synergist flexor muscle showed adaptation at moderate force levels. In contrast, application of forces using torque waveforms, which do not have a static hold phase, produced sustained discharges in muscle synergies with little adaptation. Firing frequencies reflected the magnitude of ground reaction forces, were graded to changes in force amplitude and could also be modulated by transient force perturbations added to the waveforms. Comparison of synergist activation by torques and ramp and hold functions revealed a strong influence of force dynamics (dF/dt). These studies support the idea that force receptors can act to synchronously tune muscle synergies to the range of force magnitudes and dynamics that occur in each leg according to their specific use in behavior
Erscheinungsjahr
2018
Zeitschriftentitel
Journal of Neurophysiology
Band
120
Ausgabe
4
Seite(n)
1807-1823
ISSN
0022-3077
eISSN
1522-1598
Page URI
https://pub.uni-bielefeld.de/record/2931605

Zitieren

Zill SN, Dallmann CJ, Büschges A, Chaudhry S, Schmitz J. Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli. Journal of Neurophysiology. 2018;120(4):1807-1823.
Zill, S. N., Dallmann, C. J., Büschges, A., Chaudhry, S., & Schmitz, J. (2018). Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli. Journal of Neurophysiology, 120(4), 1807-1823. doi:10.1152/jn.00371.2018
Zill, Sasha N., Dallmann, Chris J., Büschges, Ansgar, Chaudhry, Sumaiya, and Schmitz, Josef. 2018. “Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli”. Journal of Neurophysiology 120 (4): 1807-1823.
Zill, S. N., Dallmann, C. J., Büschges, A., Chaudhry, S., and Schmitz, J. (2018). Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli. Journal of Neurophysiology 120, 1807-1823.
Zill, S.N., et al., 2018. Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli. Journal of Neurophysiology, 120(4), p 1807-1823.
S.N. Zill, et al., “Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli”, Journal of Neurophysiology, vol. 120, 2018, pp. 1807-1823.
Zill, S.N., Dallmann, C.J., Büschges, A., Chaudhry, S., Schmitz, J.: Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli. Journal of Neurophysiology. 120, 1807-1823 (2018).
Zill, Sasha N., Dallmann, Chris J., Büschges, Ansgar, Chaudhry, Sumaiya, and Schmitz, Josef. “Force dynamics and synergist muscle activation in stick insects. The effects of using joint torques as mechanical stimuli”. Journal of Neurophysiology 120.4 (2018): 1807-1823.

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97 References

Daten bereitgestellt von Europe PubMed Central.

Load rather than length sensitive feedback contributes to soleus muscle activity during human treadmill walking.
af Klint R, Mazzaro N, Nielsen JB, Sinkjaer T, Grey MJ., J. Neurophysiol. 103(5), 2010
PMID: 20237313
Segment specificity of load signal processing depends on walking direction in the stick insect leg muscle control system.
Akay T, Ludwar BCh, Goritz ML, Schmitz J, Buschges A., J. Neurosci. 27(12), 2007
PMID: 17376989
Reaction to disturbances of a walking leg during stance.
Bartling C, Schmitz J., J. Exp. Biol. 203(Pt 7), 2000
PMID: 10708641

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0
Single perturbations cause sustained changes in searching behavior in stick insects.
Berg E, Buschges A, Schmidt J., J. Exp. Biol. 216(Pt 6), 2012
PMID: 23197090
A leg-local neural mechanism mediates the decision to search in stick insects.
Berg EM, Hooper SL, Schmidt J, Buschges A., Curr. Biol. 25(15), 2015
PMID: 26190069
Stick insect locomotion in a complex environment: climbing over large gaps.
Blaesing B, Cruse H., J. Exp. Biol. 207(Pt 8), 2004
PMID: 15010478

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0

Cruse, J Exp Biol 181(), 1993
A load-based mechanism for inter-leg coordination in insects.
Dallmann CJ, Hoinville T, Durr V, Schmitz J., Proc. Biol. Sci. 284(1868), 2017
PMID: 29187626
Load-regulating mechanisms in gait and posture: comparative aspects.
Duysens J, Clarac F, Cruse H., Physiol. Rev. 80(1), 2000
PMID: 10617766
The flexion synergy, mother of all synergies and father of new models of gait.
Duysens J, De Groote F, Jonkers I., Front Comput Neurosci 7(), 2013
PMID: 23494365
Active sensing without efference copy: referent control of perception.
Feldman AG., J. Neurophysiol. 116(3), 2016
PMID: 27306668
What is the biological basis of sensorimotor integration?
Flanders M., Biol Cybern 104(1-2), 2011
PMID: 21287354
In vivo measurement of ligament/tendon strains and forces: a review.
Fleming BC, Beynnon BD., Ann Biomed Eng 32(3), 2004
PMID: 15095807
Static and Dynamic Adaptation of Insect Photoreceptor Responses to Naturalistic Stimuli.
French AS, Immonen EV, Frolov RV., Front Physiol 7(), 2016
PMID: 27826250
Leg design in hexapedal runners.
Full RJ, Blickhan R, Ting LH., J. Exp. Biol. 158(), 1991
PMID: 1919412
Crossed reflex reversal during human locomotion.
Gervasio S, Farina D, Sinkjær T, Mrachacz-Kersting N., J. Neurophysiol. 109(9), 2013
PMID: 23427302
A novel computational framework for deducing muscle synergies from experimental joint moments.
Gopalakrishnan A, Modenese L, Phillips AT., Front Comput Neurosci 8(), 2014
PMID: 25520645
Biological attachment devices: exploring nature's diversity for biomimetics.
Gorb SN., Philos Trans A Math Phys Eng Sci 366(1870), 2008
PMID: 18192171

AUTHOR UNKNOWN, 0
Positive force feedback in human walking.
Grey MJ, Nielsen JB, Mazzaro N, Sinkjaer T., J. Physiol. (Lond.) 581(Pt 1), 2007
PMID: 17331984
Adaptive changes in locomotor control after partial denervation of triceps surae muscles in the cat.
Gritsenko V, Mushahwar V, Prochazka A., J. Physiol. (Lond.) 533(Pt 1), 2001
PMID: 11351036
Body side-specific control of motor activity during turning in a walking animal.
Gruhn M, Rosenbaum P, Bockemuhl T, Buschges A., Elife 5(), 2016
PMID: 27130731

AUTHOR UNKNOWN, 0
Structure and function of the elastic organ in the tibia of a tenebrionid beetle.
Ichikawa T, Toh Y, Sakamoto H., Naturwissenschaften 103(5-6), 2016
PMID: 27118185
The rate of information transfer of naturalistic stimulation by graded potentials.
Juusola M, de Polavieja GG., J. Gen. Physiol. 122(2), 2003
PMID: 12860926

AUTHOR UNKNOWN, 0
Control of position and movement is simplified by combined muscle spindle and Golgi tendon organ feedback.
Kistemaker DA, Van Soest AJ, Wong JD, Kurtzer I, Gribble PL., J. Neurophysiol. 109(4), 2012
PMID: 23100138
Relevance of in vivo force measurements to human biomechanics.
Komi PV., J Biomech 23 Suppl 1(), 1990
PMID: 2081741

AUTHOR UNKNOWN, 0
Controlling a system with redundant degrees of freedom. I. Torque distribution in still standing stick insects.
Levy J, Cruse H., J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 194(8), 2008
PMID: 18642005
Contribution of afferent feedback to the soleus muscle activity during human locomotion.
Mazzaro N, Grey MJ, Sinkjaer T., J. Neurophysiol. 93(1), 2004
PMID: 15356177
Kinematic responses to changes in walking orientation and gravitational load in Drosophila melanogaster.
Mendes CS, Rajendren SV, Bartos I, Marka S, Mann RS., PLoS ONE 9(10), 2014
PMID: 25350743
Simple robot suggests physical interlimb communication is essential for quadruped walking.
Owaki D, Kano T, Nagasawa K, Tero A, Ishiguro A., J R Soc Interface 10(78), 2012
PMID: 23097501
Assessing sensory function in locomotor systems using neuro-mechanical simulations.
Pearson K, Ekeberg O, Buschges A., Trends Neurosci. 29(11), 2006
PMID: 16956675

Pearson, J Exp Biol 56(), 1972
Sensorimotor gain control: a basic strategy of motor systems?
Prochazka A., Prog. Neurobiol. 33(4), 1989
PMID: 2682784
Positive force feedback control of muscles.
Prochazka A, Gillard D, Bennett DJ., J. Neurophysiol. 77(6), 1997
PMID: 9212270
Common motor mechanisms support body load in serially homologous legs of cockroaches in posture and walking.
Quimby LA, Amer AS, Zill SN., J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 192(3), 2005
PMID: 16362305
Climbing favours the tripod gait over alternative faster insect gaits.
Ramdya P, Thandiackal R, Cherney R, Asselborn T, Benton R, Ijspeert AJ, Floreano D., Nat Commun 8(), 2017
PMID: 28211509
Encoding of forces by cockroach tibial campaniform sensilla: implications in dynamic control of posture and locomotion.
Ridgel AL, Frazier SF, DiCaprio RA, Zill SN., J. Comp. Physiol. A 186(4), 2000
PMID: 10798724
Adaptive motor behavior in insects.
Ritzmann RE, Buschges A., Curr. Opin. Neurobiol. 17(6), 2007
PMID: 18308559

AUTHOR UNKNOWN, 0
Design and Testing of a Bionic Dancing Prosthesis.
Rouse EJ, Villagaray-Carski NC, Emerson RW, Herr HM., PLoS ONE 10(8), 2015
PMID: 26285201
Descending influences on escape behavior and motor pattern in the cockroach.
Schaefer PL, Ritzmann RE., J. Neurobiol. 49(1), 2001
PMID: 11536194

Schmitz, J Exp Biol 183(), 1993
Feasible muscle activation ranges based on inverse dynamics analyses of human walking.
Simpson CS, Sohn MH, Allen JL, Ting LH., J Biomech 48(12), 2015
PMID: 26300401

Stolz, 2015
A New Perspective on Predictive Motor Signaling.
Straka H, Simmers J, Chagnaud BP., Curr. Biol. 28(5), 2018
PMID: 29510116
Neuromechanical model of praying mantis explores the role of descending commands in pre-strike pivots.
Szczecinski NS, Martin JP, Bertsch DJ, Ritzmann RE, Quinn RD., Bioinspir Biomim 10(6), 2015
PMID: 26580957
Mechanosensation and Adaptive Motor Control in Insects.
Tuthill JC, Wilson RI., Curr. Biol. 26(20), 2016
PMID: 27780045

von, 1971
Control of climbing behavior in the cockroach, Blaberus discoidalis. II. Motor activities associated with joint movement.
Watson JT, Ritzmann RE, Pollack AJ., J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 188(1), 2002
PMID: 11935230
Hand interactions in rapid grip force adjustments are independent of object dynamics.
White O, Dowling N, Bracewell RM, Diedrichsen J., J. Neurophysiol. 100(5), 2008
PMID: 18768641

AUTHOR UNKNOWN, 0
Determining muscle's force and action in multi-articular movement.
Zajac FE, Gordon ME., Exerc Sport Sci Rev 17(), 1989
PMID: 2676547
Three-dimensional graphic reconstruction of the insect exoskeleton through confocal imaging of endogenous fluorescence.
Zill S, Frazier SF, Neff D, Quimby L, Carney M, DiCaprio R, Thuma J, Norton M., Microsc. Res. Tech. 48(6), 2000
PMID: 10738318
Load sensing and control of posture and locomotion.
Zill S, Schmitz J, Buschges A., Arthropod structure & development. 33(3), 2004
PMID: IND43653725
Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus.
Zill SN, Buschges A, Schmitz J., J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 197(8), 2011
PMID: 21544617
Directional specificity and encoding of muscle forces and loads by stick insect tibial campaniform sensilla, including receptors with round cuticular caps
Zill SN, Ansgar Buschges , Josef Schmitz , Sumaiya Chaudhry ., Arthropod structure & development. 42(6), 2013
PMID: IND600862974
Force feedback reinforces muscle synergies in insect legs
Zill SN, Ansgar Buschges , Josef Schmitz , Sumaiya Chaudhry ., Arthropod structure & development. 44(6), 2015
PMID: IND605438202
Positive force feedback in development of substrate grip in the stick insect tarsus
Zill SN, Annelie Exter , Ansgar Buschges , Josef Schmitz , Sumaiya Chaudhry ., Arthropod structure & development. 43(5), 2014
PMID: IND605438148
Effects of force detecting sense organs on muscle synergies are correlated with their response properties.
Zill SN, Neff D, Chaudhry S, Exter A, Schmitz J, Buschges A., Arthropod Struct Dev 46(4), 2017
PMID: 28552666
Force encoding in stick insect legs delineates a reference frame for motor control.
Zill SN, Schmitz J, Chaudhry S, Buschges A., J. Neurophysiol. 108(5), 2012
PMID: 22673329
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