Summary
In Manduca sexta larvae, sensory neurons innervating planta hairs on the tips of the prolegs make monosynaptic excitatory connections with motoneurons innervating proleg retractor muscles. Tactile stimulation of the hairs evokes reflex retraction of the proleg. In this study we examined activity-dependent changes in the amplitude of the excitatory postsynaptic potentials (EPSPs) evoked in a proleg motoneuron by stimulation of individual planta hair sensory neurons. Deflection of a planta hair caused a phasic-tonic response in the sensory neuron, with a mean peak instantaneous firing frequency of >300 Hz, and a tonic firing rate of 10–20 Hz. Direct electrical stimulation was used to activate individual sensory neurons to fire at a range of frequencies including those observed during natural stimulation of the hair. At relatively low firing rates (e.g., 1 Hz), EPSP amplitude was stable indefinitely. At higher instantaneous firing frequencies (>10 Hz), EPSPs were initially facilitated, but continuous stimulation led rapidly to synaptic depression. High-frequency activation of a sensory neuron could also produce post-tetanic potentiation, in which EPSP amplitude remained elevated for several min following a stimulus train. Facilitation, depression, and post-tetanic potentiation all appeared to be presynaptic phenomena. These activity-dependent changes in sensory transmission may contribute to the behavioral plasticity of the proleg withdrawal reflex observed in intact insects.
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Abbreviations
- ACh :
-
acetylcholine
- AChE :
-
acetylcholine esterase
- CNS :
-
central nervous system
- EPSP :
-
excitatory postsynaptic potential
- I h :
-
injected hyperpolarizing current
- LTP :
-
long-term potentiation
- PPR :
-
principal planta retractor motoneuron
- PTP :
-
post-tetanic potentiation
- R in :
-
input resistance
- V h :
-
hyperpolarized potential
- V m :
-
membrane potential
- VN :
-
ventral nerve
- VNA :
-
anterior branch of the ventral nerve
- V r :
-
resting potential.
References
Atwood HL (1976) Organization and synaptic physiology of crustacean neuromuscular systems. Prog Neurobiol 7:291–391
Atwood HL, Wojtowicz JM (1986) Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses. Int Rev Neurobiol 28:275–362
Atwood HL, Swenarchuk LE, Gruenweld CR (1975) Long-term synaptic facilitation during sodium accumulation in nerve terminals. Brain Res 100:198–204
Bacon JP, Altman JS (1977) A silver intensification method for cobalt filled neurones in wholemount preparations. Brain Res 138:359–363
Bell RA, Joachim FA (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69:365–373
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
Breer H, Knipper M (1984) Characterization of acetylcholine release from insect synaptosomes. Insect Biochem 14:337–344
Brogan RT, Pitman RM (1981) Axonal regeneration in an identified insect motoneurone. J Physiol (Lond) 319:34–35
Byrne JH (1982) Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica. J Neurophysiol 48:431–438
Callee JJ (1974) Synaptic transmission in the central nervous system of insects. In: Treherne JE (ed) Insect neurobiology. North Holland, Amsterdam, pp 119–185
Callee JJ, Guillet JC, Pichon Y, Boistel J (1971) Further studies on synaptic transmission in insects. II. Relations between sensory information and its synaptic integration at the level of a single giant axon in the cockroach. J Exp Biol 55:123–149
Charlton MP, Smith SG, Zucker RS (1982) Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J Physiol (Lond) 323:173–193
Cohen JL, Weiss K, Kupfermann I (1978) Motor control of buccal muscles in Aplysia. J Neurophysiol 41:157–180
Corfas G, Dudai Y (1990) Adaptation and fatigue of a mechano-sensory neuron in wild-type Drosophila and in memory mutants. J Neurosci 10:491–499
David JA, Sattelle DB (1984) Actions of cholinergic pharmacological agents on the cell body membrane of the fast coxal depressor motoneurone of the cockroach (Periplaneta americana). J Exp Biol 108:119–136
French AS (1988) Transduction mechanisms of mechanosensilla. Ann Rev Entomol 33:39–58
Gnatzy W, Tautz J (1980) Ultrastructure and mechanical properties of an insect mechanoreceptor: Stimulus-transmitting structures and sensory apparatus of the cereal filiform hairs of Gryllus. Cell Tissue Res 213:441–463
Heitler WJ, Burrows M (1977) The locust jump. II. Neural circuits of the motor programme. J Exp Biol 66:221–241
Holder RED, Sattelle DB (1972) A multiway non-return valve for use in physiological experiments. J Physiol (Lond) 226:2–3
Hue B, Lapied B, Malecot CO (1989) Do presynaptic muscarinic receptors regulate acetylcholine release in the central nervous system of the cockroach Periplaneta americana? J Exp Biol 142:447–451
Jacobs GA, Weeks JC (1990) Postsynaptic changes at a sensory-tomotoneuron synapse contribute to the developmental loss of a reflex behavior during insect metamorphosis. J Neurosci 10:1341–1356
Jones SW, Adams PH (1987) The M-current and other potassium currents of vertebrate neurons. In: Kaczmarek LK, Levitan IB (eds) Neuromodulation: The biochemical control of neuronal excitability. Oxford University Press, New York: pp 159–186
Katz PS, Harris-Warrick RM (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion. J Neurophysiol 62:571–581
Katz PS, Eigg MH, Harris-Warrick RM (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells. J Neurophysiol 62:558–570
Knipper M, Breer H (1988) Subtypes of muscarinic receptors in insect nervous system. Comp Biochem Physiol 90C:275–280
Koketsu K, Yamada M (1982) Presynaptic muscarinic receptors inhibiting active acetylcholine release in the bullfrog sympathetic ganglion. Br J Pharmacol 77:75–82
Lev-Tov A, Rahamimoff R (1980) A study of tetanic and post-tetanic potentiation of miniature endplate potentials at the frog neuromuscular junction. J Physiol (Lond) 309:247–273
Levine RB, Murphey RK (1980) Pre- and postsynaptic inhibition of identified giant interneurons in the cricket (Acheta domesticus). J Comp Physiol 135:269–282
Levine RB, Weeks JC (1989) Reorganization of neural circuits and behavior during insect metamorphosis. In: Carew TJ, Kelley DB (eds) Perspectives in neural systems and behavior. Alan R. Liss, Inc., New York, pp 195–228
Lloyd DPC (1949) Post-tetanic potentiation of response in monosynaptic reflex pathways of the spinal cord. J Gen Physiol 33:147–170
Lutz EM, Tyrer NM (1988) Immunohistochemical localization of serotonin and choline acetyltransferase in sensory neurons of the locust. J Comp Neurol 267:335–342
Magleby KL (1973a) The effect of repetitive stimulation on facilitation of transmitter release at the frog neuromuscular junction. J Physiol (Lond) 234:327–352
Magleby KL (1973b) The effect of tetanic and post-tetanic potentiation on facilitation of transmitter release at the frog neuromuscular junction. J Physiol (Lond) 234:353–371
Magleby KL, Stevens CF (1972) The effect of voltage on the time course of end-plate currents. J Physiol (Lond) 223:151–171
Magleby KL, Zengel JE (1975) A dual effect of repetitive stimulation on post-tetanic potentiation of transmitter release at the frog neuromuscular junction. J Physiol (Lond) 245:163–182
Magleby KL, Zengel JE (1976) Augmentation: a process that acts to increase transmitter release at the frog neuromuscular junction. J Physiol (Lond) 257:449–470
Marder E (ed) (1989) Modulation of neural networks underlying behavior. Saunders, Philadelphia, Sem Neurosci 1:1–79
Miyazaki S (1980) The ionic mechanism of action potentials in neurosecretory cells and non-neurosecretory cells of the silkworm. J Comp Physiol 140:43–52
Mochida S, Kobayashi H (1986) Activation of M2-muscarinic receptors causes an alteration of action potentials by modulation of calcium entry in isolated sympathetic neurons of rabbits. Neurosci Lett 72:199–204
Mochida S, Kobayashi H (1988) GTP-binding proteins mediate the M2-muscarinic effect on the action potential in isolated sympathetic neurons of rabbits. Neurosci Lett 93:247–252
Newlin SA, Schlapfer WT, Barondes SH (1980a) Separate serotonin and dopamine receptors modulate the duration of PTP at an Aplysia synapse without affecting other aspects of neurotransmission. Brain Res 181:89–106
Newlin SA, Schlapfer WT, Barondes SH (1980b) Heterosynaptic stimulation modulates the duration of PTP at an Aplysia synapse without affecting other aspects of neurotransmission. Brain Res 181:107–125
Ohmori H (1982) Development of post-tetanic potentiation at identified inhibitory and excitatory synapses in Aplysia. J Physiol 322:223–240
Pahapill PA, Lnenicka GA, Atwood HL (1987) Long-term facilitation and low-frequency depression in a crayfish phasic motor axon. J Comp Physiol A 161:367–375
Pearson KG, Goodman CS (1981) Presynaptic inhibition of transmission from identified interneurons in locust central nervous system. J Neurophysiol 45:501–515
Peterson BA, Weeks JC (1988) Somatotopic mapping of sensory neurons innervating mechanosensory hairs on the larval prolegs of Manduca sexta. J Comp Neurol 275:128–144
Pflüger HJ (1980) The function of hair sensilla on the locust's leg: The role of tibial hairs. J Exp Biol 87:163–175
Robertson RM, Pearson KG (1985) Neural circuits in the flight system of the locust. J Neurophysiol 53:110–128
Rosenthal J (1969) Post-tetanic potentiation at the neuromuscular junction of the frog. J Physiol (Lond) 203:121–133
Ryall RW (1978) Presynaptic inhibition. Trends Neurosci 1:164–166
Shepherd D, Murphey RK (1986) Competition regulates the efficacy of an identified synapse in crickets. J Neurosci 6:3152–3160
Shepherd D, Kämper G, Murphey RK (1988) The synaptic origins of receptive field properties in the cricket cereal sensory system. J Comp Physiol A 162:1–11
Suter C, Usherwood PNR (1985) Action of acetylcholine and antagonists on somata isolated from locust central neurons. Comp Biochem Physiol 80:221–229
Teyler TJ, DiScenna P (1987) Long-term potentiation. Annu Rev Neurosci 10:131–161
Trimmer BA, Weeks JC (1987) Pharmacological studies of an identified monosynaptic cholinergic sensory to motoneuron connection in the nicotine-resistant insect Manduca sexta. Soc Neurosci Abstr 13:1255
Trimmer BA, Weeks JC (1988) Cholinergic modulation of an identified motoneuron and its afferent input in the nicotine-resistant insect Manduca sexta. Soc Neurosci Abstr 14:381
Trimmer BA, Weeks JC (1989a) Effects of nicotinic and muscarinic agents on an identified motoneurone and its direct afferent inputs in larval Manduca sexta. J Exp Biol 144:303–337
Trimmer BA, Weeks JC (1989b) Characterization of an aflerent-induced change in the excitability of an insect motoneuron. Soc Neurosci Abstr 15:26
Walters ET, Byrne JH (1985) Long-term enhancement produced by activity-dependent modulation of Aplysia sensory neurons. J Neurosci 5:662–672
Weeks JC, Ernst-Utzschneider K (1989) Respecification of larval proleg motoneurons during metamorphosis of the tobacco hornworm, Manduca sexta: segmental dependence and hormonal regulation. J Neurobiol 20:569–592
Weeks JC, Jacobs GA (1987) A reflex behavior mediated by monosynaptic connections between hair afferents and motoneurons in the larval tobacco hornworm, Manduca sexta. J Comp Physiol A 160:315–329
Weeks JC, Truman JW (1984) Neural organization of peptide-activated ecdysis behaviors during the metamorphosis of Manduca sexta. II. Retention of the proleg motor pattern despite loss of the prolegs at pupation. J Comp Physiol A 155:423–433
Weeks JC, Truman JW (1985) Independent steroid control of the fates of motoneurons and their muscles during insect metamorphosis. J Neurosci 5:2290–2300
Zucker RS (1987) Neurotransmitter release and its modulation. In: Kaczmarek LK, Levitan IB (eds) Neuromodulation: The biochemical control of neuronal excitability. Oxford University Press, New York, pp 243–263
Zucker RS, Bruner J (1977) Long-lasting depression and the depletion hypothesis at crayfish neuromuscular junctions. J Comp Physiol 121:223–240
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Trimmer, B.A., Weeks, J.C. Activity-dependent induction of facilitation, depression, and post-tetanic potentiation at an insect central synapse. J Comp Physiol A 168, 27–43 (1991). https://doi.org/10.1007/BF00217101
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DOI: https://doi.org/10.1007/BF00217101