Inhibitory motoneurons in arthropod motor control: organisation, function, evolution

Allgäuer C, Honegger H-W (1993) The antennal motor system of crickets: modulation of muscle contractions by a common inhibitor, DUM neurons and proctolin. J Comp Physiol A 173:485–494 Atwood HL (1973) Crustacean motor units. In: Stein RB, Pearson KG, Smith RS, Redford JB (eds) Control of posture and locomotion. Plenum Press, New York, pp 87–104 Atwood HL, Tse FW (1988) Changes in binomial parameters of quantal release at crustacean motor axon terminals during presynaptic inhibition. J Physiol 402:177–193 Atwood HL, Tse FW (1993) Physiological aspects of presynaptic inhibition. Adv Neural Sci 1:19–65 Atwood HL, Parnas I, Wiersma CAG (1967) Inhibition in crustacean phasic neuromuscular systems. Comp Biochem Physiol 20:163–177 Atwood HL, Stevens JK, Marin L (1984) Axo-axonal synapse location and consequences for presynaptic inhibition in crustacean motor axon terminals. J Comp Neurol 225:64–74 Ballantyne D, Rathmayer W (1981) On the function of the common inhibitory neurone 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 Verlag, Berlin, pp 1–169 Baxter DA, Bittner GD (1991) Synaptic plasticity of crayfish neuromuscular junctions: presynaptic inhibition. Synapse 7:244–251 Bazemore AW, Elliott KAC, Florey E (1957) Isolation of factor I. J Neurochem 1:334–338 Bévengut M, Cournil I (1990) Gamma aminobutyric acid-inhibitory motor innervation of leg muscles of the shore crab. Eur J Neurosci 2:132–139 Bévengut M, Cattaert D, Clarac F (1996) Synaptic connections of the common inhibitory motoneurone within the fifth thoracic ganglion of crayfish. J Comp Physiol A 178:337–350 Böser S (1999) GABA-Immuncytochemie bei Acheta domesticus unter veränderten Gravitationsbedingungen. Diploma thesis, University of Karlsruhe, Germany Bräunig P, Schmäh M, Wolf H (2006) Common and specific inhibitory motor neurons innervate the intersegmental muscles in the locust thorax. J Exp Biol 209:1827–1836 Burns MD, Usherwood PNR (1979) The control of walking in orthoptera: II. Motor neurone activity in normal 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 (1996) The neurobiology of an insect brain. Oxford University Press, Oxford, pp 1–682 Burrows M, Matheson T (1994) A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor. J Neurosci 14:272–282 Calas-List D, Clare AJ, Komissarova A, Nielsen TA, Matheson T (2014) Motor inhibition affects the speed but not accuracy of aimed limb movements in an insect. J Insect Physiol 34:7509–7521 Cattaert D, El Manira A, Clarac F (1992) Direct evidence for presynaptic inhibitory mechanisms in crayfish sensory afferents. J Neurophysiol 67:610–624 Cattaert D, Bévengut M, Clarac F (1993) Synaptic connections between sensory afferents and the common inhibitory motoneuron in crayfish. J Comp Physiol A 172:71–79 Clarac F, Cattaert D (1996) Invertebrate presynaptic inhibition and motor control. Exp Brain Res 112:163–180 Clarac F, Pearlstein E (2007) Invertebrate preparations and their contribution to neurobiology in the second half of the 20th century. Brain Res Revs 54:113–161 Cooke IRC, Macmillan DL (1983) The common inhibitory innervation of the pereiopods of the crayfish Cherax destructor. J Exp Biol 225:513–517 Drummond JM, Macmillan DL (1998) The abdominal motor system of the crayfish, Cherax destructor. II. Morphology and physiology of the deep extensor motor neurons. J Comp Physiol A 183:603–619 Dudel J, Hatt H (1976) Four types of GABA receptors in crayfish leg muscles characterized by desensitization and specific antagonist. Pfluegers Arch 364:217–222 Dudel J, Menzel R, Schmidt RF (2001) Neurowissenschaft. Springer Verlag, Berlin, Heidelberg, New York Dunlop JA, Webster M (1999) Fossil evidence, terrestrialization and arachnid phylogeny. J Arachnol 27:86–93 Dürr V, König Y, Kittmann R (2001) The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern during walking. J Comp Physiol A 187:131–144 Eisenberg BR (1983) Quantitative ultrastructure of mammalian skeletal muscle. In: Comprehensive physiology. pp 73–112 Faisal AA, White JA, Laughlin SB (2005) Ion-channel noise places limits on the miniaturization of the brain’s wiring. Curr Biol 15:1143–1149 Faulkes Z, Paul DH (1997) A map of distal leg motor neurons in the thoracic ganglia of four decapod crustacean species. Brain Behav Evol 49:162–178 Ferrero E, Wales W (1976) The mandibular common inhibitory system. I. Axon topography and the nature of coupling. J Comp Physiol 109:123–134 Fischer L, Florey E (1983) Modulation of synaptic transmission and excitation-contraction coupling in the opener muscle of the crayfish, Astacus leptodactylus, by 5-hydroxytryptamine and octopamine. J Exp Biol 102:187–198 Fischer Y, Parnas I (1996a) Activation of GABAB receptors at individual boutons of the crayfish opener neuromuscular junction produces presynaptic inhibition. J Neurophysiol 75:1377–1385 Fischer Y, Parnas I (1996b) Differential activation of two distinct mechanisms for presynaptic inhibition by a single inhibitory axon. J Neurophysiol 76:3807–3816 Florey E (1954) An inhibitory and an excitatory factor of mammalian central nervous system, and their action on a single sensory neuron. Arch Int Physiol 62:33–53 Fourtner CR, Drewes CD (1977) Excitation of the common inhibitory motor neuron: a possible role in the startle reflex of the cockroach, Periplaneta americana. J Neurobiol 8:477–489 Fuchs PA, Getting PA (1980) Ionic basis for presynaptic inhibitory potentials at the crayfish claw opener. J Neurophysiol 43:1547–1557 Gabriel JP, Scharstein H, Schmidt J, Büschges A (2003) Control of flexor motoneuron activity during single leg walking of the stick insect on an electronically controlled treadwheel. J Neurobiol 56:237–251 Grebennikov VV, Beutel RG (2002) Morphology of the minute larva of Ptinella tenella, with special reference to effects of miniaturisation and the systematic position of Ptiliidae (Coleoptera: Staphylinoidea). Arthropod Struct Dev 31:157–172 Hale JP, Burrows M (1985) Innervation patterns of inhibitory motor neurones in the thorax of the locust. J Exp Biol 117:401–413 Hartline DK, Colman DR (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Curr Biol 17:R29–R35 Harzsch S, Müller CHG, Wolf H (2005) From variable to constant cell numbers: cellular characteristics of the arthropod nervous system argue against a sister-group relationship of chelicerate and “myriapoda” but favour the mandibulata concept. Dev Genes Evol 215:53–68 Henneman E (1957) Relation between size of neurons and their susceptibility to discharge. Science 26:1345–1347 Henneman E (1985) The size principle: a deterministic output emerges from a set of probabilistic connections. J Exp Biol 115:105–112 Hille B (1984) Ionic channels of excitable membranes. Sinauer Associates, Sunderland, pp 1–486 Homberg U, Bleick A, Rathmayer W (1993) Immunocytochemistry of GABA and glutamic acid decarboxylase in the thoracic ganglion of the crab Eriphia spinifrons. Cell Tissue Res 271:279–288 Honegger H-W (1981) A preliminary note on a new optomotor response in crickets: Antennal tracking of moving targets. J Comp Physiol 142:419–421 Hooper SL, Hobbs KH, Thuma JB (2008) Invertebrate muscles: thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle. Prog Neurobiol 86:72–127 Hoyle G (1983) Forms of modulatable tension in skeletal muscles. Comp Biochem Physiol 76A:203–210 Hoyle G (1984) Neuromuscular transmission in a primitive insect: modulation by octopamine, and catch-like tension. Comp Biochem Physiol 77C:219–232 Hoyle G, Field LH (1983) Elicitation and abrupt termination of behaviourally significant catch like tension in a primitive insect. J Neurobiol 14:299–312 Huddart H, Abram RG (1969) Modification of excitation-contraction coupling in locust skeletal muscle induced by caffeine. J Exp Zool 171:49–58 Jackel C, Krenz W-D, Nagy F (1994) Bicuculline/baclofen-insensitive GABA responses in crustacean neurones in culture. J Exp Biol 191:167–193 Jahromi SS, Atwood HL (1974) Three-dimensional ultrastructure of the crayfish neuromuscular apparatus. J Cell Biol 63:599–613 Josephson RK (1993) Contraction dynamics and power output of skeletal muscle. Ann Rev Physiol 55:527–546 Kutsch W, Breidbach O (1994) Homologous structures in the nervous systems of Arthropoda. Adv Insect Physiol 24:1–113 Laughlin SB, Sejnowski TJ (2003) Communication in neuronal networks. Science 301:1870–1874 Maier L, Pette D, Rathmayer W (1986) Enzyme activities in single electrophysiologically identified crab muscle fibres. J Physiol Lond 371:191–199 Maier L, Root TM, Seyfarth E-A (1987) Heterogeneity of spider leg muscle: Histochemistry and electrophysiology of identified fibres in the claw levator. J Comp Physiol B 157:285–294 Manton SM, Harding JP (1964) Mandibular mechanisms and the evolution of arthropods. Phil Trans R Soc Lond B 247:1–183 Matheson T, Field L (1995) An elaborate tension receptor system highlights sensory complexity in the hind leg of the locust. J Exp Biol 198:1673–1689 Miwa A, Ui M, Kawai N (1991) G-protein is coupled to presynaptic glutamate and GABA receptors in lobster neuromuscular synapse. J Neurophysiol 63:173–180 Moody-Corbett F, Pasztor VM (1980) Innervation, synaptic physiology, and ultrastructure of three muscles of the second maxilla in crayfish. J Neurobiol 11:21–30 Msghina M, Atwood HL (1997) Distribution and morphology of inhibitory innervation in crayfish (Procambarus clarkii) limb and abdominal muscles. Cell Tiss Res 290:111–118 Müller A, Wolf H, Galler S, Rathmayer W (1992) Correlation of electrophysiological, histochemical, and contractional properties in fibres of the coxa rotator muscle of the locust, Locusta migratoria. J Comp Physiol B 162:5–15 Murchinson D, Larimer JL (1997) Dual output interneurons in the abdominal ganglia of the crayfish Procambarus clarkii: synaptic activation of motor outputs in both the swimmeret and abdominal positioning systems by single interneurons. J Exp Biol 150:269–293 Nagayama T (1999) Uropod common inhibitory motor neurone in the terminal abdominal ganglion of the crayfish. J Exp Zool 283:541–547 Nicoll RA, Alger BE (1979) Presynaptic inhibition: transmitter and ionic mechanisms. Int Rev Neurobiol 21:217–258 Otsuka M, Iversen LL, Hall ZW, Kravitz EA (1966) Release of gamma-aminobutyric acid from inhibitory nerves of lobster. Proc Natl Acad Sci USA 56:1110–1115 Page KL, Zakotnik J, Dürr V, Matheson T (2008) Motor control of aimed limb movements in an insect. J Neurophysiol 99:484–499 Pearce J, Govind CK (1993) Reciprocal axo-axonal synapses between the common inhibitor and excitor motoneurons in crustacean limb muscles. J Neurocytol 22:259–265 Pearlstein E, Cattaert D, Clarac F (1997) Crayfish sensory terminals and motor neurones exhibit two distinct types of GABA receptors. J Comp Physiol A 180:71–79 Pearlstein E, Watson AHD, Bévengut M, Cattaert D (1998) Inhibitory connections between antagonistic motor neurones of the crayfish walking legs. J Comp Neurol 399:241–254 Pearson KG, Bergmann SJ (1969) Common inhibitory motoneurons in insects. J Exp Biol 50:445–471 Pflüger H-J, Stevenson PA (2005) Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34:379–396 Pringle JWS (1978) The Croonian lecture, 1977. Stretch activation of muscle: function and mechanism. Proc Roy Soc Lond B Biol Sci 201:107–130 Radnikow G, Bässler U (1991) Function of a muscle whose apodeme travels through a joint moved by other muscles: why the retractor unguis muscle in stick insects is tripartite and has no antagonist. J Exp Biol 157:87–99 Rathmayer W (1990) Inhibition through neurons of the common inhibitor type (CI-neurons) in crab muscles. In: Wiese K, Krenz WD, Tautz J, Reichert H, Mulloney B (eds) Frontiers in crustacean neurobiology. Birkhäuser Verlag, Basel, pp 271–278 Rathmayer W (1997) Die Bedeutung hemmender Muskelinnervation für die Lokomotion der Arthropoden. Leopoldina 43:221–235 Rathmayer W, Bévengut M (1986) The common inhibitory neuron innervates every leg muscle in crabs. J Comp Physiol A 158:665–668 Rathmayer W, Djokai S (2000) Presynaptic inhibition and the participation of GABAA receptors at neuromuscular junctions of the crab Eriphia spinifrons. J Comp Physiol A 186:287–298 Rathmayer W, Erxleben C (1983) Identified muscle fibres in a crab. I. Characteristics of excitatory and inhibitory neuromuscular transmission. J Comp Physiol 152:411–429 Rathmayer W, Hammelsbeck M (1985) Identified muscle fibres in a crab. II. Differences in facilitation properties. J Exp Biol 116:291–300 Rathmayer W, Maier L (1987) Muscle fibre types in crabs: studies on single identified muscle fibres. Am Zool 27:1067–1077 Rehfeldt C, Stickland NC, Fiedler I, Wegner J (1999) Environmental and genetic factors as sources of variation in skeletal muscle fibre number. Basic Appl Myol 9:235–253 Ritzmann R, Camhi JM (1978) Excitation of leg motor neurons by giant interneurons in the cockroach Periplaneta americana. J Comp Physiol 125:305–316 Rudomin P (1990) Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord. Trends Neurosci 13:499–505 Rykebusch S, Laurent G (1993) Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. J Neurophysiol 69:1583–1595 Schmäh M, Wolf H (2003) Inhibitory motor neurones supply body wall muscles in the locust abdomen. J Exp Biol 206:445–455 Schmidt J, Rathmayer W (1993) Central organization of common inhibitory motoneurons in the locust: role of afferent signals from leg mechanoreceptors. J Comp Physiol A 172:447–456 Schmidt-Nielsen K (2002) Scaling: why is animal size so important?. Cambridge University Press, Cambridge, pp 1–256 Seipel K, Schmid V (2005) Evolution of striated muscle: Jellyfish and the origin of triploblasty. Dev Biol 282:14–26 Selen LP, Franklin DW, Wolpert DM (2009) Impedance control reduces instability that arises from motor noise. J Neurosci 29:12606–12616 Smith DO (1978) Ultrastructural specificity of synaptic sites in nerve terminals mediating both presynaptic and postsynaptic inhibition. J Comp Neurol 182:839–849 Snodgrass RE (1950) Comparative studies on the jaws of mandibulate arthropods. Smithsonian Misc Collns 116:1–85 Tse FW, Marin L, Jahromi SS, Atwood HL (1991) Variation in terminal morphology and presynaptic inhibition at crustacean neuromuscular junctions. J Comp Neurol 304:135–146 Wales W, Ferrero E (1976) The mandibular common inhibitory system. II. Input sensitivity. J Comp Physiol 109:135–146 Walrond JP, Wiens TJ, Govind CK (1990) Inhibitory innervation of a lobster muscle. Cell Tissue Res 260:421–429 West GB, Woodruff WH, Brown JH (2002) Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proc Natl Acad Sci 99:2473–2478 Wiens TJ (1985) Triple innervation of the crayfish opener muscle: the astacuran common inhibitor. J Neurobiol 16:183–191 Wiens TJ (1989) Common and specific inhibition in leg muscles of decapods: sharpened distinctions. J Neurobiol 20:458–469 Wiens TJ (1991) Dual inhibition of the crayfish’s closer muscle by the stretcher and common inhibitors. Soc Neurosci Abstr 17:1389 Wiens TJ (1993) The closer muscle is a second target for the stretcher inhibitory motoneuron of the crayfish’s thoracic limbs. J Comp Physiol A 173:435–444 Wiens TJ, Atwood HL (1975) Dual inhibitory control in crab leg muscles. J Comp Physiol 99(3):211–230 Wiens TJ, Atwood HL (1978) Motoneuron interactions in crayfish claw control: evidence from intracellular recording. J Comp Physiol 124:237–247 Wiens TJ, Rathmayer W (1985) The distribution of the common inhibitory neuron in brachyuran limb musculature. I. Target muscles. J Comp Physiol A 156:305–313 Wiens TJ, Wolf H (1993) The inhibitory motoneurons of crayfish thoracic limbs: identification, structures, and homology with insect common inhibitors. J Comp Neurol 336:261–278 Wiens TJ, Maier L, Rathmayer W (1988) The distribution of the common inhibitory neuron in brachyuran limb musculature. II. Target fibres. J Comp Physiol A 163:651–664 Wiersma CAG (1941) The inhibitory nerve supply of the leg muscles of different decapod crustaceans. J Comp Neurol 74:63–79 Wieser W (1995) Die Optimierung des Energie und Stoffhaushalts von Zellen durch die Evolution. Biol unserer Zeit 25:140–145 Wolf H (1990) Activity patterns of inhibitory motoneurons and their impact on leg movement in tethered walking locusts. J Exp Biol 152:281–304 Wolf H (1995) Plasticity in insect leg motor control: interactions between central program and sensory signal processing. Verh Dtsch Zool Ges 88:153–164 Wolf H, Harzsch S (2002a) Evolution of the arthropod neuromuscular system. 1. Arrangement of muscles and excitatory innervation in the walking legs of a scorpion: Vaejovis spinigerus (Wood, 1863), Vaejovidae, Scorpiones, Arachnida. Arthropod Struct Dev 31:185–202 Wolf H, Harzsch S (2002b) Evolution of the arthropod neuromuscular system. 2. Inhibitory innervation of the walking legs of a scorpion: Vaejovis spinigerus (Wood, 1863), Vaejovidae, Scorpiones, Arachnida. Arthropod Struct Dev 31:203–215 Wolf H, Lang D (1994) Origin and clonal relationship of common inhibitory motoneurons CI1, and CI3 in the locust CNS. J Neurobiol 25:846–864 Wong J, Wilson ET, Malfait N, Gribble PL (2009) Limb stiffness is modulated with spatial accuracy requirements during movement in the absence of destabilizing forces. J Neurophysiol 101:1542–1549 Worden MK, Camacho JA (2006) Dual inhibition of the dactyl opener muscle in lobster. J Exp Biol 209:1385–1394 Yamawaki Y, Ishibashi W (2014) Antennal pointing at a looming object in the cricket Acheta domesticus. J Insect Physiol 60:80–91