Summary
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1.
In order to gain insight into the role of the suboesophageal ganglion ofLocusta migratoria in flight control, seven interneurons originating in the suboesophageal ganglion were recorded during flight. Their activity patterns and their contribution to flight initiation were examined. During flight, three interneurons (288, 388, 488) were tonically excited, three interneurons (397, 398, 399) were tonically inhibited and one interneuron (576) was rhythmically active.
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2.
The three interneurons 288, 388 and 488 had activity patterns similar to those described for the mesothoracic interneurons termed 404 by Pearson et al. (1985b). These interneurons discharged tonically during flight. Two of them (288, 388) received indirect excitatory input from interneurons 404, and 488 excited indirectly the neurons 404. Intracellular stimulation of 488 evoked several cycles of flight.
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3.
The interneurons 397 and 398 were phasically excited at the onset of flight but tonically inhibited during flight. 397 received direct excitatory input from a G-neuron and directly excited an elevator motoneuron as well as a local non-spiking interneuron. 398 was excited phasic-tonically by wind blown on the head and was indirectly inhibited by the neurons 404. Intracellular stimulation of 398 inhibited the mesothoracic and metathoracic subalar motoneurons, decreased the cycle frequency of flight and sometimes stopped flight altogether.
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4.
The interneuron 399 was inhibited prior to the onset of flight and remained tonically inhibited. It was inhibited by antennal stimulation, by the 404 neurons and by the rhythmically active suboesophageal ganglion interneuron 576. Intracellular stimulation of 399 inhibited a small unit in the subalar muscle (129), decreased the cycle frequency of flight and sometimes also stopped flight. In two cases flight was initiated in the quiescent locust following the cessation of 399 stimulation. At this time spikes were suppressed in 399.
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5.
Interactions between the interneurons inhibited during flight were found. Intracellular stimulation of 397 excited indirectly 398 and inhibited indirectly 399.
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6.
It is concluded that interneurons in the suboesophageal ganglion contribute to flight control. The interneurons described in this study contributed to three aspects of flight initiation. 488 influenced the activity of the flight initiating interneurons 404 (Pearson et al. 1985 b), 397 and 398 contributed to the initial response of flight motoneurons, and finally 398 and 399 contributed to flight initiation by disinhibiton of the flight system.
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References
Altman JS, Kien J (1979) Suboesophageal neurons involved in head movements and feeding in locusts. Proc R Soc Lond B 205:209–227
Arbas EA (1986) Control of hindlimb posture by wind-sensitive hairs and antennae during locust flight. J Comp Physiol A 159:849–857
Bicker G, Pearson KG (1985) Initiation of flight by stimulation of a single identified wind sensitive neuron (TCG) in the locust. J Exp Biol 104:289–294
Boyan GS (1985) Auditory input to the flight system of the locust. J Comp Physiol A 156:79–91
Boyan GS, Altman JS (1985) The suboesophageal ganglion a ‘missing link’ in the auditory pathway of the locust. J Comp Physiol A 156:413–428
Boyan GS, Ashman S, Ball EE (1986) Initiation and modulation of flight by a single giant interneuron in the cercal system of the locust. Naturwissenschaften 73:272–274
Brady J (1967) Histological observations on circadian changes in the neurosecretory cells of cockroach suboesophageal ganglion. J Insect Physiol 13:201–213
Brodfuehrer PD, Friesen WO (1986a) Initiation of swimming activity by trigger neurons in the leech suboesophageal ganglion. I. Output connections of Tr1 and Tr2. J Comp Physiol A 159:489–502
Brodfuehrer PD, Friesen WO (1986b) Initiation of swimming activity by trigger neurons in the leech suboesophageal ganglion. II. Role of segmental swim-initiating interneurons. J Comp Physiol A 159:503–510
Brodfuehrer PD, Friesen WO (1986c) Initiation of swimming activity by trigger neurons in the leech suboesophageal ganglion. III. Sensory inputs to Tr1 and Tr2. J Comp Physiol A 159:511–519
Brodfuehrer PD, Friesen WO (1986d) Control of leech swimming activity by the cephalic ganglia. J Neurobiol 17:697–705
Burrows M (1985) Nonspiking and spiking local interneurons in the locust. In: Selverston AI (ed) Model neural networks and behavior. Plenum Press, New York London
Camhi JM (1969) Locust wind receptors: III. Contribution to flight initiation and lift control. J Exp Biol 50:363–374
Camhi JM, Hinkle M (1972) Attentiveness to sensory stimuli: Central control in locusts. Science 175:550–553
Davis WJ (1976) Organizational concepts in the central motor networks of invertebrates. Adv Behav Biol 18:265–292
Davis WJ, Kennedy D (1972) Command interneurons controlling swimmeret movements in the lobster. I. Types of effects on motoneurons. J Neurophysiol 35:1–12
Eaton RC, Lavender WA, Wieland CM (1982) Alternative neural pathways initiate fast-start responses following lesions of the Mauthner neuron in goldfish. J Comp Physiol 145:485–496
Gewecke M, Philippen J (1978) Control of the horizontal flight course by air current sense organs inLocusta migratoria. Physiol Entomol 3:43–52
Gillette R, Kovac MP, Davis WJ (1982) Control of feeding motor output by paracerebral neurons in brain ofPleurobranchaea californica. J Neurophysiol 47:885–908
Granzow B, Kater SB (1977) Identified higher order neurons controlling the feeding motor programm ofHelisoma. Neuroscience 2:1049–1063
Hedwig B (1986) On the role in stridulation of plurisegmental interneurons of the acridid grasshopperOmocestus viridulus L. I. Anatomy and physiology of descending cephalothoracic interneurons. J Comp Physiol A 158:413–427
Hedwig B, Pearson KG (1984) Patterns of synaptic input to identified flight motoneurons in the locust. J Comp Physiol A 154:745–760
Horsmann U, Heinzel HG, Wendler G (1983) The phasic influence of self-generated air currents on the locust flight motor. J Comp Physiol 150:427–438
Huber F (1960) Experimentelle Untersuchungen zur nervösen Atmungsregulation der Orthopteren (Saltatoria: Gryllidae). Z Vergl Physiol 43:359–391
Kalmring K (1975) The afferent auditory pathway in the ventral cord ofLocusta migratoria (Acrididae). I. Synaptic connectivity and information processing among the auditory neurons of the ventral cord. J Comp Physiol 104:103–141
Kien J (1983) The initiation and maintenance of walking in the locust: an alternative to the command concept. Proc R Soc Lond B 219:137–174
Kien J, Altman JS (1984) Descending interneurons from the brain and suboesophageal ganglion and their role in the control of locust behaviour. J Insect Physiol 30:54–72
Kien J, Fletcher WA, Altman JS, Ramirez JM, Roth U (in press) The anatomical organization of intersegmental interneurons in the locust suboesophageal ganglion. Proc R Soc Lond B
Kovac MP, Davis WS, Matera EM, Croll RP (1983) Organization of synaptic inputs to paracerebral feeding command interneurons ofPleurobranchaea californica. I. Excitatory inputs. J Neurophysiol 49:1517–1538
Krämer K, Markl H (1978) Flight-inhibition on ground contact in the American cockroachPeriplaneta americana. I. Contact receptors and a model for their central connections. J Insect Physiol 24:577–586
Krogh A, Weis-Fogh (1951) The respiratory exchange of the desert locust (Schistocerca gregaria) before, during and after flight. J Exp Biol 28:344–357
Kupfermann I, Weiss KR (1978) The command neuron concept. Behav Brain Sci 1:3–39
Lennard PR, Getting PA, Hume RI (1980) Central pattern generator mediating swimming inTritonia. II. Initiation, maintenance and termination. J Neurophysiol 44: 165–173
Marquart V (1985) Auditorische Interneurone im thorakalen Nervensystem von Heuschrecken: Morphologie, Physiologie und synaptische Verbindungen. PhD thesis, University of Bochum, FRG
Mayer RJ, Candy DJ (1969) Control of haemolymph lipid concentration during locust flight: an adipokinetic hormone from the corpora cardiaca. J Insect Physiol 15:611–620
McClellan AD (1983) Higher order neurons in the cerebral ganglia ofPleurobranchaea have diverse effects on buccal motor patterns. J Comp Physiol 153:533–541
Möhl B (1985) Sensory aspects of flight pattern generation in the locust. In: Gewecke M, Wendler G (eds) Insect locomotion. Parey, Berlin Hamburg, pp 139–148
Moore D, Larimer JL (1987) Neural control of a cyclic postural behaviour in the crayfish,Procambarus clarkii: the patterninitiating interneurons. J Comp Physiol A 160:169–179
Nusbaum MP, Kristan WB Jr (1986) Swim initiation in the leech by serotonin-containing interneurons, cells 21 and 61. J Exp Biol 122:277–302
Olson GC, Krasne FB (1981) The crayfish lateral giants as command neurons for escape behavior. Brain Res 214:89–100
Orchard I, Lange AB (1983) The hormonal control of haemolymph lipid during flight inLocusta migratoria. J Insect Physiol 29:639–642
Otto D, Weber T (1982) Interneurons descending from the cricket cephalic ganglia that discharge in the pattern of two motor rhythms. J Comp Physiol 148:209–219
Pearson KG, Wolf H (1987) Comparison of motor patterns in the intact and deafferented flight system of the locust. I. Electromyographic analysis. J Comp Physiol A 160:259–268
Pearson KG, Reye DN, Robertson RM (1983) Phase-dependent influences of wing stretch receptor on flight rhythm in the locust. J Neurophysiol 49:1168–1181
Pearson KG, Boyan GS, Bastiani M, Goodman CS (1985a) Heterogeneous properties of segmentally homologous interneurons in the ventral nervous cord of locusts. J Comp Neurol 233:133–145
Pearson KG, Reye DN, Parsons DW, Bicker G (1985b) Flight initiating interneurons in the locust. J Neurophysiol 53:910–934
Pearson KG, Gynther IC, Heitier WJ (1986) Coupling of flight initiation to the jump in locusts. J Comp Physiol A 158:81–89
Pfau HK, Nachtigall W (1981) Der Vorderflügel grosser Heuschrecken als Luftkrafterzeuger. II. Zusammenspiel von Muskeln und Gelenkmechanik bei der Einstellung der Flügelgeometrie. J Comp Physiol 142:135–140
Pond CM (1972) Neuromuscular activity and wing movements at the start of flight ofPeriplaneta americana andSchistocerca gregaria. J Comp Physiol 78:192–209
Ramirez JM (1986) Interneuronal control of locust flight. PhD thesis, University of Regensburg, FRG
Reichert H, Rowell CHF (1985) Integration of non-phase locked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1201–1218
Ritzmann RE, Pollack AJ (1986) Identification of thoracic interneurons that mediate giant interneuron-to-motor pathways in the cockroach. J Comp Physiol A 159:639–654
Ritzmann RE, Tobias ML, Fourtner CR (1980) Flight activity initiated via giant interneurons of the cockroach: evidence for bifunctional trigger interneurons. Science 210:443–445
Ritzmann RE, Pollack AJ, Tobias ML (1983) Flight activity mediated by intracellular stimulation of dorsal giant interneurons of the cockroachPeriplaneta americana. J Comp Physiol 147:313–322
Robertson RM, Pearson KG (1982) A preparation for the intracellular analysis of neuronal activity during flight in the locust. J Comp Physiol 146:311–320
Robertson RM, Pearson KG (1983) Interneurons in the flight system of the locust: distribution, connections and resetting properties. J Comp Neurol 215:33–50
Robertson RM, Pearson KG (1984) Interneuronal organization in the flight system of the locust. J Insect Physiol 30:95–101
Robertson RM, Pearson KG (1985) Neural circuits in the flight system of the locust. J Neurophysiol 53:110–128
Rock MK, Hackett JT, Brown DL (1981) Does the Mauthner cell conform to the criteria of the command neuron concept? Brain Res 204:21–27
Ronacher B, Helversen D von, Helversen O von (1986) Routes and stations in the processing of auditory directional information in the CNS of a grasshopper, as revealed by surgical experiments. J Comp Physiol A 158:363–374
Rowell CHF (1964) Central control of an insect segmental reflex. I. Inhibition by different parts of the central nervous system. J Exp Biol 41:559–572
Rowell CHF, Reichert H (1986) Three descending interneurons reporting deviation from course in the locust. II. Physiology. J Comp Physiol A 158:775–794
Siegler MVS (1981) Postural changes alter synaptic interactions between non-spiking interneurons and motoneurons of the locust. J Neurophysiol 46:310–323
VanMarrewijk WJA, VanDenBroek ATM, Beenakkers AMT (1980) Regulation of glycogenolysis in the locust body during flight. Insect Biochem 10:675–679
Weeks JC (1982a) Synaptic basis of swim initiation in the leech. I. Connections of a swim initiating neuron (cell 204) with motor neurons and pattern-generating ‘oscillator’ neurons. J Comp Physiol 148:253–263
Weeks JC (1982b) Synaptic basis of swim initiation in the leech. II. A pattern generating neuron (cell 208) which mediates motor effects of swim initiating neuron. J Comp Physiol 148:265–279
Wendler G (1974) The influence of proprioceptive feedback on locust flight coordination. J Comp Physiol 88:173–200
Wendler G (1983) The locust flight system: Functional aspects of sensory input and methods of investigation. In: Nachtigall W (ed) BIONA-report 2. Akad Wiss Mainz, Fischer, Stuttgart New York, pp 113–125
Willows AOD (1981) Physiological basis of feeding behavior inTritonia diomedea. II. Neuronal mechanisms. J Neurophysiol 44:489–861
Wilson DM (1961) The central nervous control of flight in a locust. J Exp Biol 38:471–490
Wine JJ (1984) The structural basis of an innate behavioural pattern. J Exp Biol 112:283–319
Wolf H, Pearson KG (1987) Comparison of motor patterns in the intact and deafferented flight system of the locust. II. Intracellular recordings from flight motoneurons. J Comp Physiol A 160:269–279
Worm RAA, Beenakkers AMT (1980) Regulation of substrate utilization in the flight muscle of the locust,Locusta migratoria, during flight. Insect Biochem 10:53–59
Zarnack W (1982) Untersuchungen zum Flug von Wanderheuschrecken. Die Bewegungen, räumlichen Lagebeziehungen sowie Formen und Profile von Vorder- und Hinterflügeln. In: Nachtigall W (ed): Biona-report 1. Akad Wiss Mainz, Fischer, Stuttgart New York, pp 79–102
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Ramirez, JM. Interneurons in the suboesophageal ganglion of the locust associated with flight initiation. J. Comp. Physiol. 162, 669–685 (1988). https://doi.org/10.1007/BF01342642
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DOI: https://doi.org/10.1007/BF01342642