Abstract
Nerve cells specialized for the release of peptide hormones to the circulation, i.e., classic neurosecretory cells, retain their full complement of neuronal properties. Their activity is under control of the CNS through excitatory and inhibitory synaptic mediation. They integrate these influences with their own capabilities for endogenous activity to ultimately generate action potentials propagated to the secretory terminals. They represent the “final neuroendocrine pathway” (Knowles, 1974; E. Scharrer, 1965). In this chapter, I wish to examine the relationship between those action potentials that are propagated to the secretory terminals and release of peptide hormones from them. How much of the extensive, detailed knowledge of the mechanisms governing the release of transmitters at synapses (for reviews, see, for example, Katz, 1969; Gerschenfeld, 1973) is applicable to release of peptides from neurosecretory terminals? Are there modifications of the electrical activity of neurosecretory cells, particularly their terminals, that are related to peptide secretion? For example, is the longer duration of action potentials, well documented for the neuron somata, also a feature of neurosecretory axons and terminals, and what is its significance? What is the significance for hormone release of the “spontaneous” activity often recorded from neurosecretory cells, and of firing in bursts or patterned activity?
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Alving, B. O., 1968, Spontaneous activity in isolated somata of Aplysia pacemaker neurons, J. Gen. Physiol 45:29–45.
Andrews, P.M., Copeland, D.E., and Fingerman, M., 1971, Ultrastructural study of the neurosecretory granules in the sinus gland of the blue crab Callinectes sapidus, Z. Zeilforsch. 113:461–471.
Arch, S., 1972, Polypeptide secretion from the isolated parietovisceral ganglion of Aplysia californica, J. Gen. Physiol. 59:47–59.
Baker, P.F., Hodgkin, A.L., and Ridgeway, E.B., 1971, Depolarization and calcium entry in squid giant axons, J. Physiol. London 218:709–755.
Barker, J.L., and Gainer, H., 1975a, Studies on bursting pacemaker potential activity in molluscan neurons. I. Membrane properties and ionic contributions, Brain Res. 84:461–477.
Barker, J.L., and Gainer, H., 1975b, Studies on bursting pacemaker potential activity in molluscan neurons. II. Regulation by divalent cations, Brain Res. 84:479–500.
Barker, J.L., Ifshin, M.S., and Gainer, H., 1975, Studies on bursting pacemaker potential activity in molluscan neurons. III. Effects of hormones, Brain Res. 84:501–513.
Barrett, E., and Barrett, J.N., 1976, Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones, J. Physiol. 255:737–774.
Berlind, A., 1972, Teleost caudal neurosecretory system; release of urotensin II from isolated urophyses, Gen. Comp. Endocrinol. 18:557–560.
Berlind, A., 1976, Cellular dynamics in invertebrate neurosecretory systems, Int. Rev. Cytol. in press.
Berlind, A., and Cooke, I.M., 1968, Effect of calcium omission on neurosecretion and electrical activity of crab pericardial organs, Gen. Comp. Endocrinol. 11:458–463.
Berlind, A., and Cooke, I.M., 1970, Release of a neurosecretory hormone as peptide by electrical stimulation of crab pericardial organs, J. Exp. Biol. 53:679–686.
Berlind, A., and Cooke, I.M., 1971, The role of divalent cations in electrically elicited release of neurohormone from crab pericardial organs, Gen Comp. Endocrinol. 17:60–72.
Berlind, A., Cooke, I.M., and Goldstone, M.W., 1970, Do the monoamines in crab pericardial organs play a role in peptide secretion? J. Exp. Biol. 53:669–677.
Bern, H., and Mason, C., 1976, Cellular biology of the neurosecretory neuron, in: Handbook of Physiology, American Physiology Society, Washington, D.C., in press.
Bliss, D.E., and Welsh, J.H., 1952, The neurosecretory system of brachyuran Crustacea, Biol. Bull. 103:157–169.
Bunt, A.H., and Ashby, E.A., 1967, Ultrastructure of the sinus gland of the crayfish Procambarus clarkii, Gen. Comp. Physiol. 9:334–342.
Bunt, A., and Ashby, E., 1968, Ultrastructural changes in the crayfish sinus gland following electrical stimulation, Gen. Comp. Endocrinol. 10:376–382.
Cook, D.J., and Milligan, J.V., 1972, Electrophysiology and histology of the medial neurosecretory cells in adult male cockroaches, Periplaneta americana, J. Insect. Physiol. 18:1197–1214.
Cooke, I.M., 1964, Electrical activity and release of neurosecretory material in crab pericardial organs, Comp. Biochem. Physiol. 13:353–366.
Cooke, I.M., 1967, Potentials recorded intracellularly from neurosecretory terminals, Amer. Zool. 7:732–733.
Cooke, I.M., 1971, Calcium dependent depolarizing responses recorded from crab neurosecretory terminals, Proc. Int. Union Physiol. Sci. 9:119.
Cross, B.A., 1974, The neurosecretory impulse, in: Neurosecretion—The Final Neuroendocrine Pathway (F. Knowles and L. Vollrath, eds.), pp. 115–128, Springer-Verlag, New York.
Cross, B.A., Dyball, R.E.J., Dyer, R.G., Jones, C.W., Lincoln, D.W., Morris, J.F., and Pickering, B.T., 1975, Endocrine neurons, Recent Prog. Horm. Res. 31:243–286.
Daniel, A.R., and Lederis, K., 1967, Release of neurohypophysial hormones in vitro, J. Physiol. 190:171–187.
del Castillo, J., and Katz, B., 1954, Statistical factors involved in neuromuscular facilitation and depression, J. Physiol. 124:574–585.
Dicker, S.E., 1966, Release of vasopressin and oxytocin from isolated pituitary glands of adult and new-born rats, J. Physiol. 185:429–444.
Douglas, W.W., 1968, Stimulus-secretion coupling: The concept and clues from chromaffin and other cells, Br. J. Pharmacol. 34:451–474.
Douglas, W.W., 1973, How do neurons secrete peptides? Exocytosis and its consequences, including “synaptic vesicle” formation, in the hypothalamo-neurohypophyseal system, Recent Prog. Brain Res. 39:21–38.
Douglas, W.W., and Poisner, A.M., 1964a, Stimulus-secretion coupling in a neurosecretory organ and the role of calcium in the release of vasopressin from the neurohypophysis, J. Physiol. 172:1–18.
Douglas, W.W., and Poisner, A.M., 1964b, Calcium movement in the neurohypophysis of the rat and its relation to the release of vasopressin, J. Physiol. 172:19–30.
Douglas, W.W., and Sorimachi, M., 1971, Electrically evoked release of vasopressin from isolated neurohypophyses in sodium-free media, Br. J. Pharmacol. 42:647P.
Dreifuss, J.J., and Ruf, K.B., 1972, A transpharyngeal approach to the rat hypothalamus, in: Experiments in Physiology and Biochemistry (G. Kerkut, ed.), pp. 213–228, Academic, London.
Dreifuss, J., Kalnins, I., Kelly, J.S., and Ruf, K.B., 1971, Action potentials and release of neurohypophysial hormones in vitro, J. Physiol. 215:805–817.
Durand, J.B., 1956, Neurosecretory cell types and their secretory activity in the crayfish, Biol. Bull. 111:62–76.
Dyball, R.E., 1971, Oxytocin and ADH secretion in relation to electrical activity in antidromically identified supraoptic and paraventricular units, J. Physiol. 214:245–256.
Dyball, R.E., and Dyer, R.G., 1971, Plasma oxytocin concentration and paraventricular neurone activity in rats with diencephalic islands and intact brains, J. Physiol. 216:227–235.
Dyball, R.E., and Pountney, P.S., 1973, Discharge patterns of supraoptic and paraventricular neurones in rats given a 2 per cent NaCl solution instead of drinking water, J. Endocrinol. 56:91–98.
Fatt, P., and Katz, B., 1952, Spontaneous subthreshold activity at motor nerve endings, J. Physiol. 117:109–128.
Femlund, P., and Josefsson, L., 1972, Crustacean color-change hormone; amino acid sequence and chemical synthesis, Science 177:173–175.
Finlayson, L.H., and Osborne, M.P., 1975, Secretory activity of neurons and related electrical activity, in: Adv. Comp. Physiol. Biochem. 6:165–258 (O. Lowenstein, ed.), Academic Press, New York.
Fraenkenhauser, B., and Hodgkin, A.L., 1957, The action of calcium on the electrical properties of squid axons, J. Physiol. 137:218–244.
Frazier, W.T., Kandel, E.R., Kupfermann, I., Waziri, R., and Coggeshall, R.E., 1967, Morphological and functional properties of identified neurons in the abdominal ganglion of Aplysia californica, J. Neurophysiol. 30:1288–1351.
Fridberg, G., Iwasaki, S., Yagi, K., Bern, H., Wilson, D.M., and Nishioka, R., 1966, Relation of impulse conduction to electrically induced release of neurosecretory material from the urophysis of the teleost fish Tilapia mossambica, J. Exp. Zool. 161:137–150.
Gabe, M., 1966, Neurosecretion, Pergamon Press, Oxford, 872 pp.
Gainer, H., 1972a, Patterns of protein synthesis in individual, identified, molluscan neurons, Brain Res. 39:369–386.
Gainer, H., 1972b, Effects of experimentally induced diapause on the electrophysiology and protein synthesis of identified molluscan neurons, Brain Res. 39:387–402.
Gainer, H., 1972c, Electrophysiological behavior of an endogenously active neurosecretory cell, Brain Res. 39:403–418.
Geduldig, D., and Junge, D., 1968, Sodium and calcium components of action potentials in Aplysia giant neurone, J. Physiol. 199:347–365.
Gersch, M., Richter, K., Böhm, G.-A., and Stürzebecher, J., 1970, Selektive Ausschüttung von Neurohormonen nach elektrischer Reizung der Corpora Cardiaca von Periplaneta americana in vitro, J. Insect Physiol 16:1991–2013.
Gerschenfeld, H.M., 1973, Chemical transmission in invertebrate nervous systems and neuromuscular junctions, Physiol. Rev. 53:1–119.
Gillary, H.L., and Kennedy, D., 1969, Neuromuscular effects of impulse pattern in a crustacean motor neuron, J. Neurophysiol. 32:607–612.
Hagiwara, S., and Tasaki, I., 1958, A study of the mechanism of impulse transmission across the giant synapse of the squid, J. Physiol. 143:114–137.
Harris, G.W., Manabe, Y., and Ruf, K.B., 1969, A study of the parameters of electrical stimulation of unmyelinated fibres in the pituitary stalk, J. Physiol. 203:67–81.
Haylett, B.A., Weatherby, T.M., and Cooke, I.M., 1975, Electrically elicited release of neurohormone from isolated crab sinus gland and its dependence on Ca++, Physiologist 18:242.
Hayward, J.N., 1974, Physiological and morphological identification of hypothalamic magnocellular neuroendocrine cells in goldfish preoptic nucleus, J. Physiol. 239:103–124.
Hayward, J.N., 1975, Neural control of the posterior pituitary, Annu. Rev. Physiol. 37:191–210.
Hayward, J.N., and Jennings, D.P., 1973a, Activity of magnocellular neuroendocrine cells in the hypothalamus of unanaesthetized monkeys. I. Functional cell types and their anatomical distribution in the supraoptic nucleus and the internuclear zone, J. Physiol. 232:515–543.
Hayward, J.N., and Jennings, D.P., 1973b, Activity of magnocellular neuroendocrine cells in the hypothalamus of unanaesthetized monkeys II. Osmosensitivity of functional cell types in the supraoptic nucleus and the internuclear zone, J. Physiol. 232:545–572.
Hodgson, E., and Geldiay, S., 1959, Experimentally induced release of neurosecretory materials from roach corpora cardiaca, Biol. Bull. 117:275–283.
Ishida, A., 1967, The effect of tetrodotoxin on calcium-dependent link in stimulus-secretion coupling in neurohypophysis, Jpn. J. Physiol. 17:308–320.
Ishida, A., 1968, Stimulus-secretion coupling on the oxytocin release from the isolated posterior pituitary lobe, Jpn. J. Physiol. 18:471–480.
Ishida, A., 1970, The oxytocin release and the compound action potential evoked by electrical stimulation of the isolated neurohypophysis of the rat, Jpn. J. Physiol. 20:84–96.
Iwasaki, S., and Satow, Y., 1969, Spontaneous grouped discharge of secretory neuron soma in X-organ of crayfish, Procambarus clarkii, J. Physiol. Soc. Jpn. 31:629–630.
Iwasaki, S., and Satow, Y., 1971, Sodium- and calcium-dependent spike potentials in the secretory neuron soma of the X-organ of the crayfish, J. Gen. Physiol. 57:216–238.
Jahan-Parwar, B., Smith, M., and von Baumgarten, R., 1969, Activation of neurosecretory cells in Aplysia by osphradial stimulation, Amer. J. Physiol. 216:1246–1257.
Kado, R.T., 1973, Aplysia giant cell: Soma-axon voltage clamp differences, Science 182:843.
Kandel, E.R., 1964, Electrical properties of hypothalamic neuroendocrine cells, J. Gen. Physiol. 47:691–717.
Kater, S., 1968, Cardioaccelerator release in Periplaneta americana (L.) Science 160:765–767.
Kater, S., and Kaneko, C., 1972, An endogenously bursting neuron in the gastropod mollusc, Helisoma trivolvis, J. Comp. Physiol. 79:1–14.
Katz, B., 1969, The Release of Neural Transmitter Substances, Liverpool University Press, Liverpool, 60 pp.
Katz, B., and Miledi, R., 1967a, A study of synaptic transmission in the absence of nerve impulses, J. Physiol. 192:407–436.
Katz, B., and Miledi, R., 1967b, The release of acetylcholine from nerve endings by graded electric pulses, Proc. R. Soc. London Ser. B. 167:23–38.
Katz, B., and Miledi, R., 1969a, Tetrodotoxin-resistant electric activity in presynaptic terminals, J. Physiol. 203:459–487.
Katz, B., and Miledi, R., 1969b, Spontaneous and evoked activity of motor nerve endings in calcium Ringer, J. Physiol. 203:689–706.
Katz, B., and Miledi, R., 1970, Further study of the role of calcium in synaptic transmission, J. Physiol 207:789–801.
Kleinhaus, A., and Prichard, J., 1975, Calcium dependent action potentials produced in leech Retzius cells by tetraethylammonium chloride, J. Physiol. 246:351–361.
Kleinholz, L.H., 1966, Separation and purification of crustacean eyestalk hormones, Amer. Zool. 6:161–167.
Knowles, F., 1974, Twenty years of neurosecretion, in: Neurosecretion—The Final Neuroendocrine Pathway (F. Knowles and L. Vollrath, eds.), pp. 3–11, Springer-Verlag, New York.
Koketsu, K., and Nishi, S., 1969, Calcium and action potentials of bullfrog sympathetic ganglion cells, J. Gen. Physiol. 53:608–628.
Kupfermann, I., 1970, Stimulation of egg laying by extract of neuroendocrine cells (bag cells) of abdominal ganglion of Aplysia, J. Neurophysiol. 33:877–881.
Kupfermann, I., and Kandel, E.R., 1970, Electrophysiological properties and functional interconnections of two symmetrical neurosecretory clusters (bag cells) in abdominal ganglion of Aplysia, J. Neurophysiol. 33:865–876.
Kupfermann, I., and Weiss, K.R., 1976, Water regulation by a presumptive hormone contained in identified cell R15 of Aplysia, J. Gen. Physiol. 67:113–123.
Lincoln, D.W., 1974, Dynamics of oxytocin secretion, in: Neurosecretion—The Final Neuroendocrine Pathway (F. Knowles and L. Vollrath, eds.), pp. 129–133, Springer-Verlag, New York.
Lincoln, D.W., and Wakerley, J.B., 1975, Factors governing the periodic activation of supraoptic and paraventricular neurosecretory cells during suckling in the rat, J. Physiol. 250:443–461.
Llinás, R., Blinks, J.R., and Nicholson, C., 1972, Calcium transient in presynaptic terminals in squid giant synapse: Detection with aequorin, Science 176:1127–1129.
Maddrell, S., and Gee, J., 1974, Potassium-induced release of the diuretic hormones of Rhodniusprolixus and Glossina austeni: Ca dependence, time course and localization of neurohaemal areas, J. Exp. Biol. 61:155–171.
Mallart, A., and Martin, A.R., 1967, An analysis of facilitation of transmitter release at the neuromuscular junction of the frog, J. Physiol. 193:679–694.
Martin, A.R., and Pilar, G., 1964, An analysis of electrical coupling at synapses in the avian ciliary ganglion, J. Physiol. 171:454–475.
Meech, R.W., and Standen, N.B., 1975, Potassium activation in Helix aspersa neurones under voltage clamp: A component mediated by calcium influx, J. Physiol. 249:211–239.
Meves, H., and Vogel, W., 1973, Calcium inward currents in internally perfused giant axons, J. Physiol. 235:225–266.
Mikiten, T.M., and Douglas, W., 1965, Effect of calcium and other ions on vasopressin release from rat neurohypophysis stimulated electrically in vitro, Nature London 207:302.
Miledi, R., and Thies, R., 1971, Tetanic and post-tetanic rise in frequency of miniature end-plate potentials in low-calcium solutions, J. Physiol. 212:245–257.
Normann, T., 1973, Membrane potential of the corpus cardiacum neurosecretory cells of the blowfly, Calliphora erythrocephala, J. Insect Physiol. 19:303–318.
Normann, T., 1974, Calcium-dependence of neurosecretion by exocytosis, J. Exp. Biol. 61:401–409.
Normann, T., 1976, Neurosecretion by exocytosis, Int. Rev. Cytol. 45: in press.
Normann, T., and Duve, H., 1969, Experimentally induced release of a neurohormone influencing hemolymph trehalose level in Calliphora erythrocephala (Diptera), Gen. Comp. Endocrinol. 12:449–459.
Passano, L.M., 1953, Neurosecretory control of molting in crabs by the X-organ sinus gland complex, Physiol. Comp. Oecol. 3:155–189.
Pérez-González, M.D., 1957, Evidence of hormone containing granules in sinus glands of the fiddler crab Uca pugilator, Biol. Bull. 113:426–441.
Perkins, E.B., 1928, Color changes in Crustaceans, especially in Palaemonetes, J. Exp. Zool. 50:71–195.
Poisner, A.M., 1973, Stimulus-secretion coupling in the adrenal medulla and posterior pituitary gland, in: Frontiers in Neuroendocrinology (W. Ganong and L. Martini, eds.), pp. 33–59, Oxford, New York.
Potter, D.D., 1956, Observations on the neurosecretory system of portunid crabs, Ph.D. thesis, Harvard University.
Potter, D.D., 1958, Observations on the neurosecretory system of portunid crabs, in: 2, Internationales Symposium über Neurosekretion (W. Bargmann, B. Hanström, E. Scharrer, and B. Scharrer, eds.), pp. 113–118, Springer-Verlag, Berlin.
Rehm, ML, 1959, Observations on the localization and chemical constitution of neurosecretory material in nerve terminals in Carcinus maenas, Acta Histochem. 7:88–106.
Reuter, H., 1973, Divalent cations as charge carriers in excitable membranes, Prog. Biophys. Mol. Biol. 26:3–43.
Rubin, R.P., 1974, Calcium and the Secretory Process, Plenum Press, New York, 189 pp.
Scharrer, B., and Kater, S., 1969, Neurosecretion XV. An electron microscopic study of the corpora cardiaca of Periplaneta americana after experimentally induced hormone release, Z. Zellforsch. 95:177–186.
Scharrer, E., 1965, The final common pathway in neuroendocrine integration, Arch. Anat. Microsc. Morphol. Exp. 54:359–370.
Standen, N.B., 1975a, Calcium and sodium ions as charge carriers in the action potential of an identified snail neurone, J. Physiol. 249:241–252.
Standen, N.B., 1975b, Voltage-clamp studies of the calcium inward current in an identified snail neurone: Comparison with the sodium inward current, J. Physiol. 249:253–268.
Stinnakre, J., and Tauc, L., 1969, Central neuronal response to activation of osmoreceptors in the osphradium of Aplysia, J. Exp. Biol. 51:347–361.
Vincent, J.D., Arnauld, E., and Bioulac, B., 1972a, Activity of osmosensitive single cells in the hypothalamus of the behaving monkey during drinking, Brain Res. 44:371–384.
Vincent, J.D., Arnauld, E., and Nicolescu-Catargi, A., 1972b, Osmoreceptors and neurosecretory cells in the supraoptic complex of unanesthetized monkey, Brain Res. 45:278–281.
Wald, F., 1972, Ionic differences between somatic and axonal action potentials in snail giant neurones, J.Physiol. 220:267–281.
Wilkens, J.L., and Mote, M.I., 1970, Neuronal properties of the neurosecretory cells in the fly Sarcophaga bullata, Experientia 26:275–276.
Yagi, K., and Bern, H.A., 1965, Electrophysiological analysis of the response of the caudal neurosecretory system of Tilapia mossambica to osmotic manipulations, Gen. Comp. Endocrinol. 5:509–526.
Yagi, K., Bern, H.A., and Hagadorn, I.R., 1963, Action potentials of neurosecretory neurons in the leech Theromyzon rude, Gen. Comp. Endocrinol. 3:490–495.
Yamashita, H., Koisumi, K., and Brooks, C., 1970, Electrophysiological studies of neurosecretory cells in the cat hypothalamus, Brain Res. 20:462–466.
Zeballos, G.A., Thomborough, J.R., and Rothballer, A.B., 1975, Neurohypophysial electrical activity in the anesthetized cat, Neuroendocrinology 18:104–114.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1977 Plenum Press, New York
About this chapter
Cite this chapter
Cooke, I.M. (1977). Electrical Activity of Neurosecretory Terminals and Control of Peptide Hormone Release. In: Gainer, H. (eds) Peptides in Neurobiology. Current Topics in Neurobiology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-4130-7_12
Download citation
DOI: https://doi.org/10.1007/978-1-4613-4130-7_12
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-4132-1
Online ISBN: 978-1-4613-4130-7
eBook Packages: Springer Book Archive