Skip to main content

Advertisement

SpringerLink
Log in

Functional recovery following manipulation of muscles and sense organs in the stick insect leg

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

We studied functional recovery of leg posture and walking behaviour in the femur-tibia joint control system of stick insects. Leg extensions in resting animals and during walking are produced by different parts of a single extensor muscle. (a) Ablation of the muscle part responsible for fast movements prevented leg extension during the swing phase. Resting posture remained unaffected. Within a few post-operative days, extension movements recovered, provided that sensory feedback was available. Extension movements were now driven by the muscle part which in intact animals controls the resting posture only. (b) Selective ablation of this (slow) muscle part affected the resting posture, while walking was unaffected. The resting posture partly recovered during subsequent days. To test the range of functional recovery and underlying mechanisms, we additionally transected muscle motor innervation, or we inverted or ablated sensory feedback. We found that recovery was based on both muscular and neuronal mechanisms. The latter required appropriate sensory feedback for the process of recovery, but not for the maintenance of the recovered state. Our results thus indicate the existence of a sensory template that guides recovery. Recovery was limited to a behavioural range that occurs naturally in intact animals, though in different behavioural contexts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

fCO:

Femoral chordotonal organ

FT:

Femur-tibia

FETi:

Fast extensor tibiae motoneuron

SETi:

Slow extensor tibiae motoneuron

CI1 :

Common inhibitory motoneuron 1

References

  • Aubert I, Ridet JL, Gage FH (1995) Regeneration in the adult mammalian CNS: guided by development. Curr Opin Neurobiol 5:625–635

    Article  PubMed  CAS  Google Scholar 

  • Bässler D, Rathmayer W (1996) Photoinactivation of an identified motoneurone in the locust Locusta migratoria. J Exp Biol 199:2369–2382

    PubMed  Google Scholar 

  • Bässler D, Büschges A, Meditz S, Bässler U (1996) Correlation between muscle structure and filter characteristics of the muscle-joint system in three orthopteran insect species. J Exp Biol 199:2169–2183

    Google Scholar 

  • Bässler U (1967) Zur Regelung der Stellung des Femur-Tibia-Gelenkes bei der Stabheuschrecke Carausius morosus in der Ruhe und im Lauf. Kybernetik 4:18–26

    Article  PubMed  Google Scholar 

  • Bässler U (1972) Der Regelkreis des Kniesehnenreflexes bei der Stabheuschrecke Carausius morosus: Reaktionen auf passive Bewegung der Tibia. Kybernetik 12:8–20

    Article  PubMed  Google Scholar 

  • Bässler U (1974) Vom femoralen Chordotonalorgan gesteuerte Reaktionen bei der Stabheuschrecke Carausius morosus: Messung der von der Tibia erzeugten Kraft im inaktiven Tier. Kybernetik 16:213–226

    Google Scholar 

  • Bässler U (1977) Sense organs in the femur of the stick insect and their relevance to the control of position of the femur-tibia-joint. J Comp Physiol 121:99–113

    Article  Google Scholar 

  • Bässler U (1983a) Neural basis of elementary behaviour in stick insects. Springer, Berlin

    Google Scholar 

  • Bässler U (1983b) Influence of femoral chordotonal organ afferences on ecdysis and on the development of motor programs in locust larvae. Physiol Entomol 8:353–357

    Google Scholar 

  • Bässler U (1993a) The femur-tibia control system of stick-insects—a model for the study of the neural basis of joint control. Brain Res Rev 18:207–226

    Article  PubMed  Google Scholar 

  • Bässler U (1993b) The walking- and searching pattern generator of stick insects, a modular system composed of reflex chains and endogenous oscillators. Biol Cybern 69:305–317

    Article  Google Scholar 

  • Bässler U, Büschges A (1998) Pattern generation for insect walking movements—multisensory control of a locomotor program. Brain Res Rev 27:65–88

    Article  PubMed  Google Scholar 

  • Bässler U, Nothof U (1994) Gain control in a proprioceptive feedback loop as a prerequisite for working close to instability. J Comp Physiol A 175:23–33

    Article  Google Scholar 

  • Bässler U, Stein W (1996) Contributions of structure and innervation pattern of the stick insect extensor tibiae muscle to the filter characteristics of the muscle-joint system. J Exp Biol 199:2185–2198

    Google Scholar 

  • Bräunig P (1987) The satellite nervous system—an extensive neurohemal network in the locust head. J Comp Neurol 160:69–77

    Google Scholar 

  • Büschges A, Djokaj S, Bässler D, Bässler U, Rathmayer W (2000) Plasticity in the neuromuscular system of the locust tibia extensor muscle during larval development. J Neurobiol 42:148–159

    Article  PubMed  Google Scholar 

  • Cruse H (1990) What mechanisms coordinate leg movement in walking arthropods? Trends Neurosci 13:15–21

    Article  PubMed  CAS  Google Scholar 

  • Flohr H (1988) Post-lesion plasticity. Springer, Berlin

    Google Scholar 

  • Forssberg H, Hirschfeld H, Stokes VP (1991) Development of human locomotor mechanisms. In: Armstrong DM, Bush BMH (eds) Locomotor neural mechanisms in arthropods and vertebrates. Manchester University Press, Manchester

  • Fouad K, Fischer H, Büschges A (2002) Comparative psychology of motor systems. In: Gallagher M, Weiner IB (eds) Handbook of psychology, vol 3, biological psychology. Wiley, New York, pp 109–137

  • Hofmann T, Koch UT, Bässler U (1985) Physiology of the femoral chordotonal organ in the stick insect, Cuniculina impigra. J Exp Biol 114:207–223

    Google Scholar 

  • Graham D, Bässler U (1981) Effects of afference sign reversal on motor activity in walking stick insects (Carausius morosus). J Exp Biol 91:179–193

    Google Scholar 

  • Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72:77–98

    Article  PubMed  Google Scholar 

  • Kaas JH (1991) Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci 14:137–167

    Article  PubMed  CAS  Google Scholar 

  • Kittmann R, Schmitz J (1992) Functional specialization of the scoloparia of the femoral chordotonal organ in stick insects. J Exp Biol 173:91–108

    Google Scholar 

  • Marder E, Goaillard JM (2006) Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7:563–574

    Article  PubMed  CAS  Google Scholar 

  • Matheson T, Dürr V (2003) Load compensation in targeted limb movements of an insect. J Exp Biol 206:3175–3186

    Article  PubMed  Google Scholar 

  • Möhl B (1989) Sense organs and the control of flight. In: Goldsworthy GJ, Wheeler CH (eds) Insect flight. CRC Press, Boca Raton, FL, pp 75–97

    Google Scholar 

  • Möhl B (1993) ‘Biological noise’ and plasticity of sensorimotor pathways in the locust flight system. J Comp Physiol A 166:75–82

    Google Scholar 

  • Pearson KG, Fouad K, Misiaszek JE (1999) Adaptive changes in motor activity associated with functional recovery following muscle denervation in walking cats. J Neurophysiol 82:370–381

    PubMed  CAS  Google Scholar 

  • Rossignol S (2002) Locomotion and its recovery after spinal injury in animal models. Neurorehabil Neural Repair 16:201–206

    Article  PubMed  Google Scholar 

  • Schmitz J, Delcomyn F, Büschges A (1991) Oil and hook electrodes for en passant recordings from small nerves. In: Conn P (ed) Methods of neurosciences, vol 4. Academic, San Diego, pp 266–278

    Google Scholar 

  • Stein W, Sauer AE (1998) Modulation of sensorimotor pathways associated with gain changes in a posture-control network of an insect. J Comp Physiol A Sens Neural Behav Physiol 183:489–501

    Article  Google Scholar 

  • Stein W, Sauer A (1999) Physiology of vibration-sensitive afferents in the femoral chordotonal organ of the stick insect. J Comp Physiol A 184:253–263

    Article  Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry. Wiley, New York

    Google Scholar 

  • von Holst E, Mittelstaedt H (1950) Das Reafferenzprinzip: Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften 37:464–476

    Article  Google Scholar 

  • Webb B (2004) Neural mechanisms for prediction: do insects have forward models? Trends Neurosci 27:278–282

    Article  PubMed  CAS  Google Scholar 

  • Weiland G, Bässler U, Brunner M (1986) A biological feedback control system with electronic input: the artificially closed femur-tibia control system of stick insects. J Exp Biol 120:369–385

    Google Scholar 

  • Wolf H, Bässler U, Spieß R, Kittmann R (2001) The femur-tibia control system in a proscopiid (Caelifera, Orthoptera): a test for assumptions on functional basis and evolution of twig mimesis in stick insects. J Exp Biol 204:3815–3828

    PubMed  CAS  Google Scholar 

  • Wolf H, Harzsch S (2002) The neuromuscular system in the walking legs of a scorpion. 1. Arrangement of muscles and excitatory innervation. Arthropod Struct Dev 31:185–202

    Article  Google Scholar 

  • Wolf R, Heisenberg M (1990) Visual control of straight flight in Drosophila melanogaster. J Comp Physiol A 167:269–283

    Article  PubMed  CAS  Google Scholar 

  • Wolf R, Heisenberg M (1991) Basic organization of operant behaviour as revealed in Drosophila flight orientation. J Comp Physiol A 169:699–705

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Tove Heller for expert help with the backfill stainings and Ursula Seifert and Jessica Ausborn for finishing the English text. The experiments of this study comply with the “Principles of animal care”, publication No. 86-23, revised 1985, of the National Institute of Health, and with the current laws of the Federal Republic of Germany.

Author information

Authors and Affiliations

  1. Chamissostr. 16, 70193, Stuttgart, Germany

    Ulrich Bässler

  2. Institute of Neurobiology, University of Ulm, 89069, Ulm, Germany

    Harald Wolf & Wolfgang Stein

Authors
  1. Ulrich Bässler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Harald Wolf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wolfgang Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wolfgang Stein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bässler, U., Wolf, H. & Stein, W. Functional recovery following manipulation of muscles and sense organs in the stick insect leg. J Comp Physiol A 193, 1151–1168 (2007). https://doi.org/10.1007/s00359-007-0268-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-007-0268-0

Keywords

Search

Navigation