Abstract
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1.
Normal activity in bilateral pairs of heart interneurons, from ganglia 3 or 4, in the medicinal leech (Hirudo medicinalis) is antiphasic due to their reciprocally inhibitory connections. However, Ca+-free Co+-containing salines lead to synchronous oscillations in these neurons.
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2.
Internal TEA+ allows expression of full plateaus during Co++ induced oscillations in heart interneurons; these plateaus are not blocked by Cs+. Similar plateaus are also observed with internal TEA+ alone, but under these conditions activity in heart interneurons from ganglia 3 or 4 is antiphasic.
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3.
Plateaus in heart interneurons induced by Co++ and internal TEA+ involve a conductance increase.
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4.
A voltage-dependent inward current, IP, showing little inactivation, was isolated using single-electrode voltageclamp in heart interneurons. This current is carried at least in part by Na+; the current is reduced when external Na+ is reduced and is carried by Li+ when substituted for Na+.
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5.
Calcium channel blockers such as La3+ and Co++ block neither the TEA+ induced plateaus nor IP, suggesting that Na+ is not using Ca++ channels. Moreover, IP is enhanced by Ca++-free Co++-containing salines. Thus, IP is correlated with the TEA+- and Co++-induced plateau behavior.
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Abbreviations
- HEPES :
-
N-2-hydroxyethylpiperazine-N′-2-ethanesulphonic acid
- TEA :
-
tetraethylammonium
- V h :
-
holding potential
- HN :
-
heart interneuron
- SEVC :
-
single-electrode-voltage-clamp
- STX :
-
Saxitoxin
- TTX :
-
Tetrodotoxin
References
Angstadt JD, Calabrese RL (1989) A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J Neurosci 9: 2846–2857
Angstadt JD, Calabrese RL (1991) Calcium currents and graded synaptic transmission between heart interneurons of the leech. J Neurosci 11(3):746–759
Angstadt JD, Friesen WO (1991) Synchronized oscillatory activity in leech neurons induced by calcium channel blockers. J Neurophysiol 66(6): 1858–1873
Arbas EA, Calabrese RL (1987a) Ionic conductances underlying the activity of interneurons that control heartbeat in the medicinal leech. J Neurosci 7(12):3945–3952
Arbas EA, Calabrese RL (1987b) Slow oscillations of membrane potential in interneurons that control heartbeat in the medicinal leech. J Neurosci 7(12):3953–3960
Calabrese RL, Angstadt JD, Arbas EA (1989) A neural oscillator based on reciprocal inhibition. In: Carew TJ, Kelly D (eds) Perspectives in neural systems and behavior. Liss, New York, pp 33–50
Colmers WE, Lewis Jr DV, Wilson WA (1982) Cs+ loading reveals Na+-dependent persistent in current and negative slope resistance region in Aplysia giant neurons. J Neurophysiol 48(5):1191–1200
Davis RE, Stuart AE (1988) A persistent, TTX-sensitive sodium current in an invertebrate neuron with neurosecretory ultrasructure. J Neurosci 8(11);3978–3991
Hounsgaard J, Midtgaard J (1988) Intrinsic determinants of firing pattern in Purkinje cells of the turtle cerebellum in vitro. J Physiol (Lond) 402:731–749
Hille B (1992) Ionic channels of excitable membranes. Second Edition. Sinauer Associates, Sunderland, MA
Johansen J, Kleinhaus AL (1987) Saxitoxin differentiates between two types of Na+-dependent potentials in the Retzius cell of Hirudinid leeches. J Exp Biol 131:351–363
Laurent, G (1991) Evidence for voltage-activated outward currents in the neuropilar membrane of locust nonspiking local interneurons. J Neurosci 11(6): 1713–1726
Llinas R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171–195
Nicholls JG, Kuffler SW (1964) Extracellular space as a pathway for exchange between blood and neurons in the central nervous system of the leech: The ionic composition of glial cells and neurons. J Neurophysiol 27:645–671
Opdyke CA, Calabrese RL (1990) Blockade of outward current uncovers a persistent inward current in heart interneurons of the leech Hirudo medicinalis. Soc Neurosci Abstr 16:182
Peterson EL (1983) Generation and coordination of heartbeat timing oscillation in the medicinal leech. I. Oscillation in isolated ganglia. J Neurophysiol 49:611–626
Schirrmacher K, Deitmer JW (1991) Sodium- and calcium-dependent excitability of embryonic leech ganglion cells in culture. J Exp Biol 155:435–453
Schmidt J, Calabrese RL (1992) Evidence for acetylcholine as an inhibitory transmitter of heart interneurons in the leech. J Exp Biol 171:329–347
Simon TW, Opdyke CA, Calabrese RL (1992) Modulatory effects of FMRF-NH2 on outward currents and oscillatory activity in heart interneurons of the medicinal leech. J Neurosci 12(2):525–537
Thompson WJ, Stent GS (1976a) Neuronal control of heartbeat in the medicinal leech. I. Generation of the vascular constriction rhythm by heart motor neurons. J Comp Physiol 111:261–279
Thompson WJ, Stent GS (1976b) Neuronal control of heartbeat in the medicinal leech. II. Intersegmental coordination of heart motor neuron activity by heart interneurons. J Comp Physiol 111:281–307
Thompson WJ, Stent GS (1976c) Neuronal control of heartbeat in the medicinal leech. II. Synaptic relations of the heart interneurons. J Comp Physiol 111:309–333
Tolbert LP, Calabrese RL (1985) Anatomical analysis of contacts between identified neurons that control heartbeat in the leech Hirudo medicinalis. Cell Tissue Res 242:257–267
Yang J, Lent CM (1983) Calcium depletion produces Na+-dependent, sustained depolarizations of Retzius cell membranes in the leech CNS. J Comp Physiol 150:499–507
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Opdyke, C.A., Calabrese, R.L. A persistent sodium current contributes to oscillatory activity in heart interneurons of the medicinal leech. J Comp Physiol A 175, 781–789 (1994). https://doi.org/10.1007/BF00191850
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DOI: https://doi.org/10.1007/BF00191850