Abstract
Intracellular recordings of mesothoracic common inhibitory neurons (CI1, CI2 and CI3) were made while tactile hairs of the middle legs of locusts (Locusta migratoria) were mechanically stimulated. Generally the three common inhibitory neurons were excited by stimulation of tactile hairs on the ventral and dorsal surface of femur and tibia. The response pattern of all three CI neurons was similar suggesting that they work as a functional unit. Touching hairs on the dorsal surface of tibia and tarsus in some cases led to inhibition of CIs. The connection between sensory cells of tactile hairs and common inhibitory neurons is polysynaptic.
To identify interneurons which mediate afferent signals, simultaneous intracellular recordings from CIs and interneurons were made. Different spiking interneurons were identified which made excitatory or inhibitory monosynaptic connections with CIs. Interneurons with inhibitory input to CIs belonged to the ventral midline group of spiking local interneurons. Behavioral and electrophysiological results indicate that reflex movements of the leg are accompanied by activity of CI neurons. Further it appears that CI activity is inhibited when reflex movements of the leg are actively suppressed by the animal.
Similar content being viewed by others
Abbreviations
- CI:
-
common inhibitor
- IN:
-
interneuron
- LY:
-
Lucifer Yellow
References
Altman JS, Shaw MK, Tyrer NM (1980) Input synapses on a locust sensory neurone revealed by cobalt-electron microscopy. Brain Res 189:245–250
Bacon J, Altman JS (1977) A silver intensification method for cobalt-filled neurones in wholemount preparations. Brain Res 138:359–363
Ballantyne D, Rathmayer W (1981) On the function of the common inhibitory neuron in the walking legs of the crab, Eriphia spinifrons. J Comp Physiol 143:111–122
Bässler U (1983) Neural basis of elementary behavior in stick insects. Springer, Berlin Heidelberg New York
Bässler U (1986) Afferent control of walking movements in the stick insect Cuniculina impigra. J Comp Physiol A 158:351–362
Bässler U, Hoffmann T, Schuch U (1986) Assisting components within a resistance reflex of the stick insect, Cuniculina impigra. Physiol Entomol 11:359–366
Burns MD (1974) Structure and physiology of the locust femoral chordotonal organ. J Insect Physiol 20:1319–1339
Burns MD, Usherwood PNR (1979) The control of walking in Orthoptera. II. Motor neuron activity in free-walking animals. J Exp Biol 79:69–98
Burrows M (1973) Physiological and morphological properties of the metathoracic common inhibitory neuron of the locust. J Comp Physiol 82:59–78
Burrows M (1987) Parallel processing of proprioceptive signals by spiking local interneurons and motor neurons in the locust. J Neurosci 7:1864–1080
Burrows M (1989) Processing of mechanosensory signals in local reflex pathways of the locust. J Exp Biol 146:209–227
Burrows M (1992) Local cicuits for the control of leg movements in an insect. Trends Neurosci 6:226–232
Burrows M, Horridge GA (1974) The organization of inputs to motoneurons of the locust metathoracic leg. Phil Trans R Soc Lond B 269:49–94
Burrows M, Siegler MVS (1982) Spiking local interneurons mediate local reflexes. Science 217:650–652
Burrows M, Siegler MVS (1985) The organization of receptive fields of spiking local interneurons in the locust metathoracic ganglion. J Comp Neurol 224:483–508
Burrows M, Watkins BL (1986) Spiking local interneurons in the mesothoracic ganglion of the locust: homologies with metathoracic interneurons. J Comp Neurol 245:29–40
Field LH, Burrows M (1982) Reflex effects of the femoral chordotonal organ upon leg motor neurones of the locust. J Exp Biol 101:265–285
Godden DH (1972) The motor innervation of the leg musculature and motor output during thanatosis in the stick insect (Carausius morosus). J Comp Physiol 143:81–91
Hale JP, Burrows M (1985) Innervation patterns of inhibitory motor neurones in the thorax of the locust. J Exp Biol 117:401–413
Laurent G, Hustert R (1988) Motor neuronal receptive fields delimit patterns of motor activity during locomotion of the locust. J Neurosci 8:4349–4366
Kutsch W, Schneider H (1987) Histological characterization of neurons innervating functionally different muscles of locust. J Comp Neurol 261:515–528
Nagayama T (1990) The organization of receptive fields of an anteromedial group of spiking local interneurons in the locust with exteroceptive input from the legs. J Comp Physiol A 166:471–476
Nagayama T, Burrows M (1990) Input and output connections of an anteromedial group of spiking local interneurons in the metathoracic ganglion of the locust. J Neurosci 10:785–794
Pearson KG (1973) Function of peripheral inhibitory axons in insects. Am Zool 13:321–330
Pflüger H-J (1980) The function of hair sensilla on the locust's leg: the role of tibial hairs. J Exp Biol 87:163–175
Pitman RM, Tweedle CD, Cohen MJ (1972) Branching of central neurons: Intracellular cobalt injection for light and electron microscopy. Science 176:412–114
Rathmayer W, Erxleben C (1983) Identified muscle fibers in a crab. I. Characteristics of excitatory and inhibitory neuromuscular transmission. J Comp Physiol 152:411–420
Rathmayer W, Maier L. (1987) Muscle fiber types in crabs: Studies on single identified muscle fibers. Am Zool 27:1067–1077
Runion HI, Usherwood PNR (1968) Tarsal receptors and leg reflexes in the locust and grasshopper. J Exp Biol 49:421–436
Schmidt J, Rathmayer W (1989a) Common inhibitory neurones in the locust: input from sense organs of the leg and local interneurones. In: Elsner N, Singer W (eds) Dynamics and plasticity in neural systems. Proceed 17th Göttingen Neurobiology Conference. Thieme, Stuttgart New York, p 133
Schmidt J, Rathmayer W (1989b) The inhibited inhibitor: Common inhibitory neurones of the locust under sensory and interneuronal control. In: Erber J, Menzel R, Pflüger H-J, Todt D (eds) Neural mechanisms of behavior. Proceed 2nd International Congress of Neuroethology. Thieme, Stuttgart New York, p 15
Siegler MVS, Burrows M (1983) Spiking local interneurons as primary integrators of mechanosensory information in the locust. J Neurophysiol 50:1281–1295
Siegler MVS, Burrows M (1984) The morphology of two groups of spiking local interneurons in the metathoracic ganglion of the locust. J Comp Neurol 224:463–482
Siegler MVS, Burrows M (1986) Receptive fields of motor neurones underlying local tactile reflexes in the locust. J Neurosci 6:507–513
Snodgras RE (1929) The thoracic mechanism of a grasshopper, and its antecedents. Smithson Misc Coll 82:1–111
Usherwood PNR, Grundfest H (1965) Peripheral inhibition in the skeletal muscle of insects. J Neurophysiol 28:497–518
Usherwood PNR, Runion HI (1970) Analysis of the mechanical responses of metathoracic extensor tibia muscles of free-walking locusts. J Exp Biol 52:39–58
Watson AHD, Pflüger H-J (1984) The ultrastructure of prosternal sensory hair afferents within the locust central nervous system. Neuroscience 11:269–279
Watson AHD, Burrows M, Hale JP (1985) The ultrastructure of common inhibitory motor neurones in the thorax of the locust. J Comp Neurol 239:341–359
Wiens TJ (1989) Common and specific inhibition in leg muscles of decapods: sharpened distinctions. J Neurophysiol 20:458–469
Wiens TJ, Maier L, Rathmayer W (1988) The distribution of the common inhibitory neuron in brachyuran limb musculature. II. Target fibers. J Comp Physiol A 163:651–664
Wolf H (1990a) On the function of a locust flight steering muscle and its inhibitory innervation. J Exp Biol 150:55–80
Wolf H (1990b) Activity patterns of inhibitory motoneurons and their impact on leg movement in tethered walking locusts. J Exp Biol 152:281–304
Wolf H (1992) Reflex modulation in locusts walking on a treadwheel — intracellular recordings from motoneurons. J Comp Physiol A 170:443–462
Wolf H, Schmidt J (1990) Sensory input to locust common inhibitory motoneurons during walking. Verhandl Deutsch Zool Ges G Fischer, Stuttgart New York, p 437
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Schmidt, J., Rathmayer, W. Central organization of common inhibitory motoneurons in the locust: role of afferent signals from leg mechanoreceptors. J Comp Physiol A 172, 447–456 (1993). https://doi.org/10.1007/BF00213526
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00213526