Summary
In this paper, I have examined the behavioral functions of feedback loops between the cockroach (Periplaneta americana) giant interneurons (GIs) and the flight thoracic rhythm generator.
-
1.
During sequences of flight-like activity, I have recorded from identified giant interneurons from the dorsal (dGIs) or the ventral (vGIs) group and stimulated them either with current pulses or with wind stimuli delivered to the cerci.
-
2.
Removal of the dGIs' activity which normally occurs during natural flight reduced both the wingbeat frequency and flight duration, and increased the variability of the wingbeat frequency (Fig. 6). Intracellular rhythmic stimulation of a single dGI during flight increased the wingbeat frequency and the duration of flight (Figs. 7, 8). The wind sensitivity of the dGIs was unchanged during flight compared with at rest (Fig. 2). A single short burst of spikes in a dGI had complex effects on the flight muscle recording but apparently did not reset the flight rhythm (Fig. 9). These results suggest that the rhythmic activation of the dGIs during natural light participates in the control of the wingbeat frequency and the flight duration (Fig. 12).
-
3.
In contrast to the dGIs, the vGIs became significantly less sensitive to wind during flight (Fig. 3). Stimulation of one of the vGIs (GI1) with 10 spikes at roughly 180/s during flight evokes immediate cessation of flight (Figs. 10, 11). Given that the vGI activity can stop flight, the inhibition imposed on the ventral group during flight appears to be designed to prevent this group from interfering with the flight program (Fig. 12).
Similar content being viewed by others
Abbreviations
- EMG :
-
electromyogram
- dGIs :
-
dorsal giant interneurons
- vGIs :
-
ventral giant interneurons
- GI :
-
giant interneuron
- EF :
-
efferent feedback
- PSP :
-
post-synaptic potential
References
Arshavsky YI, Gelfand IM, Orlovsky G (1983) The cerebellum and control of rhythmical movements. Trends Neurosci 6:417–422
Beal SP, Langley DJ, Edwards DH (1990) Inhibition of escape tailflip in crayfish during backward walking and the defense posture. J Exp Biol 152:577–582
Bell CC (1989) Sensory coding and corollary discharge effects in mormyrid electric fish. J Exp Biol 146:229–253
Bernard J, Thomas D (1988) Distribution of glutamate decarboxylase-like immunoreactivity in the sixth abdominal ganglion of the cockroach Periplaneta americana. Cell Tissue Res 253:129–135
Bernard JB, Gobin B, Callec JJ (1983) A chordotonal organ inhibits giant interneurons in the sixth abdominal ganglion of the cockroach. J Comp Physiol 153:377–383
Blagburn JM, Sattelle DB (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
Boyan GS, Ball EE (1986) Wind-sensitive interneurons in the terminal ganglion of praying mantids. J Comp Physiol A 159:773–789
Boyan GS, Ball EE (1990) Neural organization and information processing in the wind-sensitive cercal receptor/giant interneurone system of the locust and other orthopteroid insects. Prog Neurobiol 35:217–243
Brodfuehrer PD, Friesen WO (1986) From stimulation to undulation: neural pathway for the control of swimming in the leech. Science 234:1002–1004
Callec JJ, Sattelle DB (1973) A simple technique for monitoring the synaptic actions of pharmacological agents. J Exp Biol 59:752–38
Camhi JM (1984) A case study: The escape system of the cockroach. In: Neuroethology: Nerve cells and natural behavior of animals. Sinauer, Sunderland, Massachusetts, pp 79–105
Camhi JM (1988) Escape behavior in the cockroach: Distributed neural processing. In: Camhi JM (ed) Invertebrate neuroethology, a multi-author review. Experientia 44:361–462
Comer CM (1985) Analyzing cockroaches' escape behavior with lesions of individual giant interneurons. Brain Res 335:342–346
Currie SN, Carlsen RC (1987) Modulated vibration-sensitivity of lamprey Mauthner neurons. J Exp Biol 129:41–51
Daley DL, Delcomyn F (1981) Modulation of the excitability of cockroach giant interneurons during walking. I. Simultaneous excitation and inhibition. J Comp Physiol 138:213–219
Daley DL, Vardi N, Appignani B, Camhi JM (1981) Morphology of the giant interneurons and cercal nerve projections of the American cockroach. J Comp Neurol 196:41–52
Davis WJ (1985) Central feedback loops and some implications for motor control. In: Barnes WPJ, Gladden MH (eds) Feedback and motor control in invertebrates and vertebrates. Croom Helm, London Sydney Dover, pp 13–33
Fourtner CR, Randall JB (1982) Studies on cockroach flight: The role of continuous neural activation of non-flight muscles. J Exp Zool 221:143–154
Gandevia SC (1987) Roles for perceived voluntary motor commands in motor control. Trends Neurosci 10:81–85
Grillner S (1985) Neurobiological bases of rhythmic motor acts in vertebrates. Science 228:143–149
Guthrie BL, Porter JD, Sparks DL (1983) Corollary discharge provides accurate eye position information to the oculomotor system. Science 221:1193–1195
Holst E von, Mittelstaedt H (1950) Das Reafferenzprincip. Naturwissenschaften 37:464–476
Kupfermann I, Weiss KR (1978) The command neuron concept. Behav Brain Sci 1: 3–39
Libersat F, Camhi JM (1988) Control of sensory feedback by movement during flight in the cockroach. J Exp Biol 136:483–488
Libersat F, Goldstein RS, Camhi JM (1987) Nonsynaptic regulation of sensory activity during movement in cockroaches. Proc Natl Acad Sci USA 84:8150–8154
Libersat F, Levy A, Camhi JM (1989) Multiple feedback loops in the flying cockroach: Excitation of the dorsal and inhibition of the ventral giant interneurons. J Comp Physiol A 165:651–668
Libersat F, Kiflawi M, Camhi JM (1990) Function of feedback loops between the giant interneurons and the flight circuitry in the cockroach. Soc Neurosci Abstr 16:313–16
McCasland JS, Konishi M (1981) Interaction between auditory and motor activities in avian song control nucleus. Proc Natl Acad Sci USA 78:7815–7819
Murphy RK, Palka J (1974) Efferent control of cricket giant fibres. Nature 248:249–251
Ritzmann RE (1981) Motor responses to paired stimulation of Giant Interneurons in the cockroach Periplaneta americana. II. The ventral Giant Interneurons. J Comp Physiol 143:71–80
Ritzmann RE (1984) The cockroach escape response. In: Eaton R (ed) Neural mechanisms of startle behavior. Plenum Press, New York, pp 93–131
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, Pollack AJ, Tobias ML (1982) Flight activity mediated by intracellular stimulation of dorsal giant interneurons of the cockroach Periplaneta americana. J Comp Physiol 147:313–322
Ritzmann RE, Fourtner CR, Pollack AJ (1983) Morphology and physiological identification of motor neurons innervating flight musculature in the cockroach, Periplaneta americana. J Exp Zool 225:347–356
Roberts BL, Russell IJ (1972) The activity of lateral line efferent neurons in stationary and swimming dogfish. J Exp Biol 57:435–448
Robertson RM, Pearson KG (1985) Neural circuits in the flight system of the locust. J Neurophysiol 53:110–128
Selverston AI (1976) Neuronal mechanisms for rhythmic motor pattern generation in a simple system. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds) Neuronal control of locomotion. Plenum Press, New York, pp 377–399
Selverston AI, Moulins M (1985) Oscillatory neural networks. Ann Rev Physiol 47:29–48
Stein PSG (1971) Intersegmental coordination of swimmeret motoneuron activity in crayfish. J Neurophysiol 34:310–318
Stevenson PA, Kutsch W (1987) A reconsideration of the central pattern generator concept for locust flight. J Comp Physiol A 161:115–119
Suga N, Shinozawa T (1974) Site of neural attenuation of responses to self-vocalized sounds in echolocating bats. Science 183:1211–1213
Watson AHD (1990) Ultrastructural evidence of GABAergic input onto cercal afferents in the locust (Locusta migratoria). J Exp Biol 148:509–515
Weeks JC (1982) Segmental specialization of leech swim-initiating interneuron, cell 205. J Neurosci 2:972–985
Wendler G (1974) The influence of proprioceptive feedback on locust flight coordination. J Comp Physiol 88:173–200
Westin J, Langberg JJ, Camhi JM (1977) Responses of giant interneurons of the cockroach to wind puffs of different directions and velocities. J Comp Physiol 121:307–324
Wilson DM (1961) The central nervous control of flight in the locust. J Exp Biol 38:471–490
Wine JJ, Krasne FB (1982) The cellular organization of crayfish escape behavior. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea, Vol. 4: Neural integration and behavior. Academic Press, New York, pp 241–292
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Libersat, F. Modulation of flight by the giant interneurons of the cockroach. J Comp Physiol A 170, 379–392 (1992). https://doi.org/10.1007/BF00191427
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00191427