Skip to main content
Log in

Distributed processing on the basis of parallel and antagonistic pathways simulation of the femur-tibia control system in the stick insect

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

In inactive stick insects, sensory information from the femoral chordotonal organ (fCO) about position and movement of the femur-tibia joint is transferred via local nonspiking interneurons onto extensor and flexor tibiae motoneurons. Information is processed by the interaction of antagonistic parallel pathways at two levels: (1) at the input side of the nonspiking interneurons and (2) at the input side of the motoneurons. We tested by a combination of physiological experiments and computer simulation whether the known network topology and the properties of its elements are sufficient to explain the generation of the motor output in response to passive joint movements, that is resistance reflexes. In reinvestigating the quantitative characteristics of interneuronal pathways we identified 10 distinct types of nonspiking interneurons. Synaptic inputs from fCO afferents onto these interneurons are direct excitatory and indirect inhibitory. These connections were investigated with respect to position and velocity signals from the fCO. The results were introduced in the network simulation. The motor output of the simulation has the same characteristics as the real system, even when particular types of interneurons were removed in the simulation and the real system.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anastasio TJ, Robinson DA (1990) Distributed parallel processing in the vertical vestibulo-ocular reflex: Learning networks compared to tensor theory. Biol. Cybern. 63:161–167.

    Google Scholar 

  • Bässler U (1976) Reversal of a reflex to a single motoneuron in the stick insect Carausius morosus. Biol. Cybern. 24:47–49.

    Google Scholar 

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

    Google Scholar 

  • Bässler U (1986) Afferent control of walking movements in the stick insect Cuniculina impigra. II. Reflex reversal and the release of swing phase in the restrained foreleg. J. Comp. Physiol. A158:351–362.

    Google Scholar 

  • Bässler U (1988) Functional principles of pattern generation for walking movements of stick insects forelegs: The role of the femoral chordotonal afferences. J. Exp. Biol. 136:125–147.

    Google Scholar 

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

    Google Scholar 

  • Bässler U, Storrer J, Saxer K (1982) The neural basis of catalepsy in the stick insect Cuniculina impigra. 2. The role of the extensor motor neuron and the characteristic of the extensor tibiae muscle. Biol. Cybern. 46:1–6.

    Google Scholar 

  • Bässler U, Hofmann T, Schuch U (1986) Assisting components within a resistance reflex of the stick insect, Cuniculina impigra. Physiol. Entomol. 11:359–366.

    Google Scholar 

  • Bässler U, Büschges A (1990) Interneurones participating in the “active reaction” in stick insects Biol. Cybern. 62:529–538.

    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. A174:23–33.

    Google Scholar 

  • Bergdoll S, Koch UT (1995) BIOSIM: A biological neural network simulator for research and teaching, featuring interactive graphical user interface and learning capabilities. Neurocomputing 8:93–112.

    Google Scholar 

  • Büschges A (1990) Nonspiking pathways in a joint-control loop of the stick insect Carausius morosus. J. Exp. Biol. 151:133–160.

    Google Scholar 

  • Büschges A (1994) The physiology of sensory cells in the ventral scoloparium of the stick insect femoral chordotonal organ. J. Exp. Biol. 189:285–292.

    Google Scholar 

  • Büschges A, Schmitz J (1991) Nonspiking pathways antagonize the resistance reflex in the thoraco-coxal joint of stick insects. J. Neurobiol. 22:224–237.

    Google Scholar 

  • Büschges A, Kittmann R, Schmitz J (1994) Identified nonspiking interneurons in leg reflexes and during walking in the stick insect. J. Comp. Physiol. A 174:685–700.

    Google Scholar 

  • Büschges A, Wolf H (1995) Nonspiking local interneurons in insect leg motor control. I. Common layout and species-specific response properties of femur-tibia joint control pathways in stick insect and locust. J. Neurophysiol. 73:1843–1860.

    Google Scholar 

  • Burrows M (1987a) Parallel processing of proprioceptive signals by spiking local interneurons and motor neurones in the locust. J. Neurosci. 7:1064–1080.

    Google Scholar 

  • Burrows M (1987b) Inhibitory interactions between spiking and nonspiking local interneurons in the locust. J. Neurosci. 7: 3282–3292.

    Google Scholar 

  • Burrows M (1989) Processing of mechanosensory signals in local reflex pathways of the locust. J. Exp. Biol. 146:209–227.

    Google Scholar 

  • Burrows M (1992) Local circuits for the control of leg movement in an insect. TINS 15:226–232.

    Google Scholar 

  • Burrows M, Laurent GJ, Field LH (1988) Proprioceptive inputs to nonspiking local interneurons contribute to local reflexes of a locust hindleg. J. Neurosci. 8:3085–3093.

    Google Scholar 

  • Burrows M, Laurent GJ (1989) Reflex circuits and the control of movement. In: R Durbin, C Miall, G Mitchison, eds. The Computing Neuron. Addison-Wesley Publishing Co., Wokingham. pp. 244–261.

    Google Scholar 

  • Burrows M, Laurent GJ (1993) Synaptic potentials in the central terminals of locust proprioceptive afferents. J. Neurosci. 13:808–819.

    Google Scholar 

  • Burrows M, Matheson T (1994) A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor. J. Neurosci. 14:272–282.

    Google Scholar 

  • Cattaert D, El Manira A, Clarac F (1992) Direct evidence for presynaptic inhibitory mechanisms in crayfish sensory afferents. J. Neurophysiol. 67:610–624.

    Google Scholar 

  • Driesang RB, Büschges A (1993) The neural basis of catalepsy in the stick insect. IV. Properties of nonspiking interneurons. J. Comp. Physiol. A 173:445–454.

    Google Scholar 

  • Driesang RB, Büschges A (1996) Physiological changes in central neuronal pathways contributing to the generation of a reflex reversal. J. Comp. Physiol. A, in press.

  • Duysens J, Trippel M, Horstmann GA, Dietz V (1990) Gating and reflex reversal of reflexes in ankle muscles during human walking. Exp. Brain. Res. 82:351–358.

    Google Scholar 

  • Ebner I, Bässler U (1978) Zur Regelung der Stellung des Femur — Tibia Gelenks im Mesothorax der Wanderheuschrecke Schistocerca gregaria (Forskal). Biol. Cybern. 29:83–96.

    Google Scholar 

  • Egelhaaf M, Borst A (1993) Motion computation and visual orientation in flies. Comp. Biochem. Physiol. 104A:659–673.

    Google Scholar 

  • El Manira A, Cattaert D, Clarac F (1991) Monosynaptic connections mediate resistance reflex in crayfish (Procambarus clarkii) walking legs. J. Comp. Physiol. A168:337–349.

    Google Scholar 

  • Frost WN, Kandel ER (1995) Structure of the network mediating siphon-elicited siphon withdrawal in Aplysia. J. Neurophysiol. 73:2413–2427.

    Google Scholar 

  • Grimm K, Sauer AE (1995) The high number of neurons contributes to the robustness of the locust flight-CPG against parameter variation. Biol. Cybern. 72:329–335.

    Google Scholar 

  • Harris-Warrick RM, Nagy F, Nusbaum MP (1992a) Neuromodulation of stomatogastric networks by identified neurons and transmitters. In: RM Harris-Warrick, E Marder, AI Selverston, M Moulins, eds. Dynamic Biological Networks: The Stomatogastric Nervous System, MIT Press, Boston, pp. 87–137.

    Google Scholar 

  • Harris-Warrick RM, Marder E, Selverston AI, Moulins M, eds. (1992b) Dynamic Biological Networks. The Stomatogastric Nervous System. MIT Press, Cambridge, Mass.

    Google Scholar 

  • Hofmann T, Koch UT (1985) Acceleration receptors in the femoral chordotonal organ of the stick insect, Cuniculina impigra. J. Exp. Biol. 114:225–237.

    Google Scholar 

  • 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 

  • Kittmann R (1991) Gain control in the femur-tibia feedback system of the stick insect. J. Exp. Biol. 157:503–522.

    Google Scholar 

  • Laurent G (1990) Voltage-dependent nonlinearities in the membrane of locust nonspiking local interneurons, and their significance for synaptic integration. J. Neurosci. 10:2268–2280.

    Google Scholar 

  • Laurent G (1991) Evidence for voltage-activated outward currents in the neuropilar membrane of locust nonspiking interneurons. J. Neurosci. 11:1713–1726.

    Google Scholar 

  • Laurent G, Seymour-Laurent KJ, Johnson K (1993) Dendritic excitability and a voltage-gated calcium current in locust nonspiking local interneurons. J. Neurophysiol. 69:1484–1498.

    Google Scholar 

  • Lockery SR, Kristan WB (1990a) Distributed processing of sensory information in the leech. I. Input-output relations of the local bending reflex. J. Neurosci. 10:1811–1815.

    Google Scholar 

  • Lockery SR, Kristan WB (1990b) Distributed processing of sensory information in the leech. II. Identification of interneurons contributing to the local bending reflex. J. Neurosci. 10:1816–1829.

    Google Scholar 

  • Matheson T (1992) Range fractionation in the locust metathoracic femoral chordotonal organ. J. Comp. Physiol. A170:509–520.

    Google Scholar 

  • McClelland JL, Rumelhart DE (1988) Parallel Distributed Processing. MIT Press, Cambridge, Mass.

    Google Scholar 

  • Morton D, Chiel H (1994) Neural architectures for adaptive behavior. TINS 17:413–420.

    Google Scholar 

  • Nagayama T, Hisada T (1987) Opposing parallel connections through crayfish local nonspiking interneurons. J. Comp. Neurol. 257:347–358.

    Google Scholar 

  • Namba H, Nagayama T, Hisada M (1994) Descending control of nonspiking local interneurons in the terminal abdominal ganglion of the crayfish. J. Neurophysiol. 72:235–247.

    Google Scholar 

  • Osborn CE, Popelle RE (1992) Parallel distributed network characteristics of the DSCT. J. Neurophysiol. 68:1100–1112.

    Google Scholar 

  • Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Ann. Rev. Neurosci. 16:265–297.

    Google Scholar 

  • Pearson KG (1995) Reflex reversal in the walking systems of mammals and arthropods. In: WR Ferrell, U Proske, eds. Neural Control of Movement. Plenum Press, New York. pp. 135–141.

    Google Scholar 

  • Pearson KG, Wong RKS, Fourtner CR (1976) Connexions between hair-plate afferents and motoneurons in the cockroach leg. J. exp. Biol. 64:251–266.

    Google Scholar 

  • Pearson KG, Ramirez JM (1992) Parallels with other invertebrate and vertebrate motor systems. In: RM Harris-Warrick, E Marder, AI Selverston, M Moulins, eds. Dynamic Biological Networks: The Stomatogastric Nervous System. MIT Press, Cambridge, MA.

    Google Scholar 

  • Prochazka A (1989) Sensorimotor gain control: A basic strategy of motor systems? Prog. Neurobiol. 33:281–307.

    Google Scholar 

  • Ritzmann RE, Pollack AJ (1990) Parallel motor pathways from thoracic interneurons of the ventral giant interneuron system of the cockroach Periplaneta americana. J. Neurobiol. 21:1219–1235.

    Google Scholar 

  • Rudomin P (1990) Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord. Trend Neurosci. 13:499–505.

    Google Scholar 

  • Sauer AE, Büschges A (1994) Presynaptic inhibition of afferents — A mechanism influencing gain in proprioceptive feedback systems. In: N Elsner, H Breer, eds. Götingen Neurobiology Report 1994. Georg Thieme Verlag Stuttgart, New York. p. 283.

    Google Scholar 

  • Sauer AE, Driesang RB, Büschges A, Bässler U (1995) Information processing in the femur-tibia control loop of stick insects 1. The response characteristics of two nonspiking interneurons result from parallel excitatory and inhibitory inputs. J. Comp. Physiol. A177:145–158.

    Google Scholar 

  • Schmitz J, Delcomyn F, Büschges A (1991) Oil and hook electrodes for en passant recording from small nerves. In: PM Conn, ed. Methods in Neuroscience 4. Academic Press, San Diego, pp. 266–278.

    Google Scholar 

  • Shepherd GM (1988) Neurobiology. 2nd ed. Oxford University Press, New York.

    Google Scholar 

  • Skorupski P, Rawat BM, Bush BMH (1992) Heterogenity and central modulation of feedback reflexes in crayfish motor pool. J. Neurophysiol. 67:648–663.

    Google Scholar 

  • Skorupski P, Sillar KT (1986) Phase-dependent reversal of reflexes mediated by the thoracocoxal muscle receptor organ in the crayfish, Pacifastacus leniusculus. J. Neurophysiol. 55:689–695.

    Google Scholar 

  • Tsau Y, Wu J-Y, Hopp H-P, Cohen LB, Schiminovich D, Falk CX (1994) Distributed aspects of the response to siphon touch in Aplysia: spread of stimulus information and cross-correlation analysis. J. Neurosci. 14:4167–4184.

    Google Scholar 

  • Weiland G, Koch UT (1987) Sensory feedback during active movements of stick insects. J. Exp. Biol. 133:137–156.

    Google Scholar 

  • Wendel O (1993) MOBIS: Ein wissensbasiertes Experimentiersystem zur Simulation biologisch orientierter neuronaler Netze. In: R Hofestädt, F Krückerberg, T Lengauer, eds. Informatik in den Biowissenschaften. Springer-Verlag, Berlin, pp. 203–213.

    Google Scholar 

  • Wolf H (1991) Sensory feedback in the locust flight patterning. In: DM Armstrong, BMH Busch, eds. Local Neuronal Mechanism in Arthropods and Vertebrates. Manchester University Press, Manchester, pp. 134–148.

    Google Scholar 

  • Wolf H, Büschges A (1995) Nonspiking local interneurons in insect local motor control. 2. The role of nonspiking local interneurons in the control of leg swing during walking. J. Neurophyiol 73:1861–1875.

    Google Scholar 

  • Wu J-Y, Cohen LB, Falk CX (1994) Neuronal activity during different behaviors in Aplysia: A distributed organization? Science 263:820–823.

    Google Scholar 

  • Zecevic D, Wu J-Y, Cohen LB, London JA, Höpp H-P, Falk CX (1989) Hundreds of neurons in the Aplysia abdominal ganglion are active during the gill-withdrawal reflex. J. Neurosc. 9:3681–3689.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sauer, A.E., Driesang, R.B., Büschges, A. et al. Distributed processing on the basis of parallel and antagonistic pathways simulation of the femur-tibia control system in the stick insect. J Comput Neurosci 3, 179–198 (1996). https://doi.org/10.1007/BF00161131

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00161131

Keywords

Navigation