Role of presynaptic inputs to proprioceptive afferents in tuning sensorimotor pathways of an insect joint control network

Journal of Neurobiology

Volumn 32, Issue 4, 1997, Pages 359-376

  Sauer, A E ^a   Buschges A ^a   Stein, W ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

picrotoxin; position and velocity sensitivity; posture control; presynaptic inhibition; stick insect

Indexed keywords

CHLORIDE ION; PICROTOXIN;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BODY POSTURE; CATALEPSY; DEPOLARIZATION; INFORMATION PROCESSING; INSECT; MEMBRANE STEADY POTENTIAL; MOTONEURON; NERVE CELL NETWORK; NONHUMAN; PRESYNAPTIC INHIBITION; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROPRIOCEPTION; SENSORIMOTOR FUNCTION; SYNAPTIC POTENTIAL; TIBIA;

AFFERENT PATHWAYS; ANIMALS; FEMALE; INSECTS; JOINTS; NEURONS, AFFERENT; PROPRIOCEPTION; SYNAPTIC TRANSMISSION;

EID: 1842403532     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199704)32:4<359::AID-NEU1>3.0.CO;2-5     Document Type: Article

References (59)

1. 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. A 121:99-113.
2. BÄSSLER, U. (1983). Neural Basis of Elementary Behavior in Stick Insects. Springer Verlag, Berlin.
3. 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. A 158:351-362.
4. 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.
5. 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 Res. Rev. 18:207-226.
6. BLAGBURN, J. M. and SATTELLE, D. B. (1987). Presynaptic depolarization mediates presynaptic inhibition at a synapse between an identified mechanosensory neurone and giant interneurone 3 in the first instar cockroach, Periplaneta americana. J. Exp. Biol. 127:135-157.
7. BURROWS, M. (1987). Parallel processing of proprioceptive signals by spiking local interneurons and motor neurones in the locust. J. Neurosci. 7:1064-1080.
8. BURROWS, M. (1992). Local circuits for the control of leg movement in an insect. Trends Neurosci. 15:226-232.
9. BURROWS, M. (1994). The influence of mechanosensory signals on the control of leg movements in an insect. In: Fortschritte der Zoologie: Vol. 39: Neural basis of behavioural adaptations. K. Schildberger and N. Elsner, Eds. Gustav Fischer Verlag, Stuttgart, pp. 145-165.
10. BURROWS, M. and LAURENT, G. J. (1993). Synaptic potentials in the central terminals of locust proprioceptive afferents. J. Neurosci. 13:808-819.
11. BURROWS, M., LAURENT, G. J., and FIELD, L. H. (1988). Proprioceptive inputs to nonspiking local interneurons contribute to local reflexes of a locust hindleg. J. Neurosci. 8:3085-3093.
12. BURROWS, M. and MATHESON, T. (1994). A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor. J. Neurosci. 14:272-282.
13. BÜSCHGES, A. (1990). Non-spiking pathways in a joint-control loop of the stick insect Carausius morosus. J. Exp. Biol. 151:133-160.
14. 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.
15. BÜSCHGES, A. (1995). Plasticity of neuronal networks that control posture and movement of leg joints in insects. Verh. Dtsch. Zool. Ges. 88:139-151.
16. BÜSCHGES, A. and HAAS, R. (1996). "Building blocks" of insect walking pattern generation: ionic basis of central rhythmic synaptic drive to leg motoneurons. Soc. Neurosc. Abstr. 59.11.
17. BÜSCHGES, A. and 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.
18. CATTAERT, D., EL MANIRA, A., and CLARAC, F. (1992). Direct evidence for presynaptic inhibitory mechanisms in crayfish sensory afferents. J. Neurophysiol. 67:610-624.
19. DEAN, J. and CRUSE, H. (1986). Evidence for the control of velocity as well as position in leg protraction and retraction by the stick insect. In: H. Heuer and C. Fromm, Eds. Generation and Modulation of Action Patterns. Springer-Verlag, Heidelberg, pp. 263-274.
20. DIXON, W. J. and MASSEY, F. J., Jr. (1969). Introduction to Statistical Analysis, 3rd ed. McGraw-Hill, New York.
21. DRIESANG, R. B. and BÜSCHGES, A. (1993). The neural basis of catalepsy in the stick insect. IV. Properties of nonspiking interneurons. J. Comp. Physiol. A 173:445-454.
22. DRIESANG, R. B. and BÜSCHGES, A. (1996). Physiological changes in central neuronal pathways contributing to the generation of a reflex reversal. J. Comp. Physiol. A 179:45-57.
23. EL MANIRA, A., CATTAERT, D., and CLARAC, F. (1991). Monosynaptic connections mediate resistance reflex in crayfish (Procambarus clarkii) walking legs. J. Comp. Physiol. A 168:337-349.
24. FIELD, L. H. and BURROWS, M. (1982). Reflex effects of the femoral chordotonal organ upon leg motor neurones of the locust. J. Exp. Biol. 102:265-285.
25. FIELD, L. H. and COLES, M. M. L. (1994). The position-dependent nature of postural resistance reflexes in the locust. J. Exp. Biol. 188:65-88.
26. FIELD, L. H. and PFLÜGER, H.-J. (1989). The femoral chordotonal organ: a bifunctional orthopteran (Locusta migratoria) sense organ? Comp. Biochem. Physiol. 93A:729-743.
27. GALLAGHER, J. P., HIGASHI, H., and NISHI, S. (1978). Characterization and ionic basis of GABA-induced depolarization recorded in vivo from cat primary afferent neurones. J. Physiol. Lond. 275:263-282.
28. GOSSARD, J.-P., CABELGUEN, J.-M., and ROSSIGNOL, S. (1977). Phase-dependent modulation of primary afferent depolarization in single cutaneous primary afférents evoked by peripheral stimulation during fictive locomotion in the cat. Brain Res. 537:14-23.
29. GRAMOLL, S. and SAUER, A. E. (1996). Characterization and modelling of outward currents in identified nonspiking interneurons involved in the femur tibia reflex loop in the stick insect. In: Göttingen Neurobiology Report 1996. N. Elsner and H.-U. Schnitzler, Eds. Georg Thieme Verlag, Stuttgart, p. 126.
30. HATSOPOULOS, N. G., BURROWS, M., and LAURENT, G. J. (1995). Hysteresis reduction in proprioception using presynaptic shunting inhibition. J. Neurophysiol. 73:1031-1042.
31. HOFMANN, T. and KOCH, U. T. (1985). Acceleration receptors in the femoral chordotonal organ of the stick insect, Cuniculina impigra. J. Exp. Biol. 114:225-237.
32. HOFMANN, T., KOCH, U. T., and BÄSSLER, U. (1985). Physiology of the femoral chordotonal organ in the stick insect, Cuniculina impigra. J. Exp. Biol. 114:207-223.
33. IVERSEN, L. L. (1984). Amino acids and peptides: fast and slow chemical signals in the nervous system? Proc. R. Soc. Lond. [Biol.] 221:245-260.
34. JANIG, W., SCHMIDT, R. F., and ZIMMERMANN, M. (1968). Two specific feedback pathways to the central afferent terminals of phasic and tonic mechanoreceptors. Exp. Brain Res. 6:116-129.
35. KENNEDY, D., CALABRESE, R. L., and WINE, J. J. (1974). Presynaptic inhibition: primary afferent depolarization in crayfish neurons. Science 186:451-454.
36. KENNEDY, D., MCVITTIE, J., CALABRESE, R., FRICKE, R. A., CRAELIUS, W., and CHIAPELLA, P. (1980). Inhibition of mechanosensory interneurons in the crayfish. I. Presynaptic inhibition from giant fibers. J. Neurophysiol. 43:1495-1509.
37. KRASNE, F. B. and BRYAN, J. S. (1973). Habituation: regulation through presynaptic inhibition. Science 182:590-592.
38. LAURENT, G. (1990). Voltage-dependent nonlinearities in the membrane of locust nonspiking local intemeurons, and their significance for synaptic integration. J. Neurosci. 10:2268-2280.
39. LAURENT, G. (1991). Evidence for voltage-activated outward currents in the neuropilar membrane of locust nonspiking interneurons. J. Neurosci. 11:1713-1726.
40. LEVINE, R. B. and MURPHEY, R. K. (1980). Pre-and post-synaptic inhibition of identified giant interneurons in the cricket (Acheta domesticus) J. Comp. Physiol. A 135:269-282.
41. PEARSON, K. G. (1995). Reflex reversal in the walking systems of mammals and arthropods. In: Neural Control of Movement. W. R. Ferell and U. Proske, Eds. London, Plenum Press, pp. 135-141.
42. PROCHAZKA, A. (1989). Sensorimotor gain control: a basic strategy of motor systems? Prog. Neurobiol. 33:281-307.
43. ROSSIGNOL, S., LUND, J. P., and DREW, T. (1988). The role of sensory inputs in regulating patterns of rhythmical movements in higher vertebrates. In: Neuronal Control of Rhythmic Movements in Vertebrates. A. H. Cohen, S. Rossignol, and S. Grillner, Eds. Wiley, New York, pp. 201-283.
44. RUDOMIN, P. (1990). Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord. Trends Neurosci. 13:499-505.
45. SAUER, A. E. and BÜSCHGES, A. (1994). Presynaptic inhibition of afferents: a mechanism influencing gain in proprioceptive feedback systems. In: Göttingen Neurobiology Report 1994. N. Elsner and H. Breer, Eds. Georg Thieme Verlag, Stuttgart, p. 283.
46. SAUER, A. E., DRIESANG, R. B., BÜSCHGES, A., and 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. A 177:145-158.
47. SAUER, A. E., DRIESANG, R. B., BÜSCHGES, A., and BÄSSLER, U. (1996). Distributed processing on the basis of parallel and antagonistic pathways. Simulation of the femur-tibia control system in the stick insect. J. Comput. Neurosc. 3:179-198.
48. SCHMIDT, R. F. (1971). Presynaptic inhibition in the vertebrate central nervous system. Ergeb. Physiol. 63:20-101.
49. SCHMITZ, J., DLCOMYN, F., and B̈SCHGES, A. (1991). Oil and hook electrodes for en passant recording from small nerves. In: Methods in Neuroscience 4. P. M. Conn, Ed. Academic Press, San Diego, pp. 266-278.
50. SILLAR, K. T. and SKORUPSKI, P. (1986). Central input to primary afferent neurones in crayfish, Pacifastus leniusculus is correlated with rhythmic output of thoracic ganglia. J. Neurophysiol. 55:678-688.
51. TAKEUCHI, A. and TAKEUCHI, N. (1969). A study of the action of picrotoxin on the inhibitory neuromuscular junction of the crayfish. J. Physiol. (Lond.) 183:418-432.
52. THEOPHILIDIS, G. and BURNS, M. D. (1990). The firing pattern of the locust (Schistocerca gregaria americana) mesothoracic femoral motor axons in resistance reflexes and during walking on a treadmill. J. Insect Physiol. 36:513-522.
53. WATSON, A. H. D. (1986). The distribution of GABA-like immunoreacitivy in the thoracic nervous system of the locust Schistocerca grigeria. Cell Tissue Res. 246:331-341.
54. WATSON, A. H. D. and BURROWS, M. (1987). Immunocytochemical and pharmacological evidence for GABA-ergic spiking local interneurones in the locust. J. Neurosci. 7:1741-1751.
55. WATSON, A. H. D. and LAURENT, G. (1990). GABA-like immunoreacitvity in a population of locust intersegmental interneurones and their inputs. J. Comp. Neurol. 302:761-767.
56. WEILAND, D. J., BÄSSLER, U., and 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.
57. WEILAND, G. and KOCH, U.T. (1987). Sensory feedback during active movements of stick insects. J. Exp. Biol. 133:137-156.
58. WOLF, H. and BURROWS, M. (1995). Proprioceptive sensory neurons of a locust leg receive rhythmic presynaptic inhibition during walking. J. Neurosci. 15:5623-5636.
59. ZILL, S. N. (1985). Plasticity and proprioception in insects. I. Responses and cellular properties of individual receptors of the locust metathoracic femoral chordotonal organ. J. Exp. Biol. 116:435-461.