Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1990 Feb;421:247–262. doi: 10.1113/jphysiol.1990.sp017943

Intraterminal recordings from the rat neurohypophysis in vitro.

C W Bourque 1
PMCID: PMC1190083  PMID: 2348393

Abstract

1. Intracellular recordings were obtained from neurosecretory terminals (endings of Herring bodies), axons and pars intermedia cells in the isolated neuro-intermediate lobe of the rat. Responses to current injection and stimulation of the neural stalk (NS) were examined at 34 degrees C. Cellular identity was verified following injection of Lucifer Yellow. 2. Neurosecretory terminals were identified by a constant-latency action potential response to NS stimulation and an appropriate collision test. This response was not blocked by Ca2(+)-free solutions. Hyperpolarization of the terminals could block the generation of a local spike. Injection of Lucifer Yellow into eleven units confirmed that such responses were recorded from neurosecretory terminals. 3. Neurohypophysial nerve terminals had a resting potential of -60.4 +/- 1.1 mV and displayed a spike amplitude of 72.4 +/- 1.9 mV. The local spike threshold was -41.6 +/- 1.9 mV. Voltage-current relations were linear near resting potential, but displayed strong outward rectification positive to -55 mV. While terminals could fire at high frequencies during NS stimulation, repetitive activity could not be evoked by prolonged depolarizing current pulses. 4. During the initial 1-3 s of a train of brief depolarizing pulses or NS stimuli, nerve terminals showed a progressive broadening of their action potentials. At steady state, the duration of these impulses increased logarithmically with firing rate, showing a maximum near 25 Hz. Spike broadening in nerve terminals was reversibly abolished by superfusion of the neural lobe with Ca2(+)-free, Mn2(+)-containing solutions. In the absence of external Ca2+, action potentials were smaller, and lacked a prominent shoulder on their repolarizing phase. 5. Sustained (greater than 5 s) repetitive stimulation at 10-20 Hz led to a gradual increase in the latency for invasion and eventual failure of the spike-generating mechanism within the terminal. This effect required several seconds to recover. In contrast, action potentials recorded within the axon followed continuous repetitive stimulation and did not show any frequency-dependent changes in duration (0.7 +/- 0.1 ms). 6. Cells of the pars intermedia (PI) displayed an input resistance of 215.7 +/- 47.4 M omega and fired a single action potential in response to current injection. The amplitude of this current-evoked spike decreased during repetitive stimulation, but its duration was not affected. In 87% of the PI cells tested, stimulation of the NS evoked a Ca2(+)-sensitive synaptic response which reversed near -40 mV, but no cell was directly activated by the stimulus.

Full text

PDF
247

Images in this article

257Fig. 10
on p.257

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Augustine G. J., Charlton M. P., Smith S. J. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J Physiol. 1985 Oct;367:163–181. doi: 10.1113/jphysiol.1985.sp015819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baertschi A. J., Dreifuss J. J. The antidromic compound action potential of the hypothalamo-neurohypophysial tract, a tool for assessing posterior pituitary activity in vivo. Brain Res. 1979 Aug 10;171(3):437–451. doi: 10.1016/0006-8993(79)91048-5. [DOI] [PubMed] [Google Scholar]
  3. Bicknell R. J., Brown D., Chapman C., Hancock P. D., Leng G. Reversible fatigue of stimulus-secretion coupling in the rat neurohypophysis. J Physiol. 1984 Mar;348:601–613. doi: 10.1113/jphysiol.1984.sp015128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bicknell R. J., Leng G. Endogenous opiates regulate oxytocin but not vasopressin secretion from the neurohypophysis. Nature. 1982 Jul 8;298(5870):161–162. doi: 10.1038/298161a0. [DOI] [PubMed] [Google Scholar]
  5. Bicknell R. J., Leng G. Relative efficiency of neural firing patterns for vasopressin release in vitro. Neuroendocrinology. 1981 Nov;33(5):295–299. doi: 10.1159/000123248. [DOI] [PubMed] [Google Scholar]
  6. Bourque C. W. Ionic basis for the intrinsic activation of rat supraoptic neurones by hyperosmotic stimuli. J Physiol. 1989 Oct;417:263–277. doi: 10.1113/jphysiol.1989.sp017800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bourque C. W., Renaud L. P. Calcium-dependent action potentials in rat supraoptic neurosecretory neurones recorded in vitro. J Physiol. 1985 Jun;363:419–428. doi: 10.1113/jphysiol.1985.sp015719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brethes D., Dayanithi G., Letellier L., Nordmann J. J. Depolarization-induced Ca2+ increase in isolated neurosecretory nerve terminals measured with fura-2. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1439–1443. doi: 10.1073/pnas.84.5.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cazalis M., Dayanithi G., Nordmann J. J. The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. J Physiol. 1985 Dec;369:45–60. doi: 10.1113/jphysiol.1985.sp015887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clarke G., Wood P., Merrick L., Lincoln D. W. Opiate inhibition of peptide release from the neurohumoral terminals of hypothalamic neurones. Nature. 1979 Dec 13;282(5740):746–748. doi: 10.1038/282746a0. [DOI] [PubMed] [Google Scholar]
  11. Davis M. D., Hadley M. E. Pars intermedia electrical potentials: changes in spike frequency induced by regulatory factors of melanocyte stimulating hormone (MSH) secretion. Neuroendocrinology. 1978;26(5):277–282. doi: 10.1159/000122783. [DOI] [PubMed] [Google Scholar]
  12. Douglas W. W., Taraskevich P. S. Calcium component to action potentials in rat pars intermedia cells. J Physiol. 1980 Dec;309:623–630. doi: 10.1113/jphysiol.1980.sp013530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dreifuss J. J., Kalnins I., Kelly J. S., Ruf K. B. Action potentials and release of neurohypophysial hormones in vitro. J Physiol. 1971 Jul;215(3):805–817. doi: 10.1113/jphysiol.1971.sp009499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dutton A., Dyball R. E. Phasic firing enhances vasopressin release from the rat neurohypophysis. J Physiol. 1979 May;290(2):433–440. doi: 10.1113/jphysiol.1979.sp012781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dyball R. E., Grossmann R., Leng G., Shibuki K. Spike propagation and conduction failure in the rat neural lobe. J Physiol. 1988 Jul;401:241–256. doi: 10.1113/jphysiol.1988.sp017160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gainer H., Wolfe S. A., Jr, Obaid A. L., Salzberg B. M. Action potentials and frequency-dependent secretion in the mouse neurohypophysis. Neuroendocrinology. 1986;43(5):557–563. doi: 10.1159/000124582. [DOI] [PubMed] [Google Scholar]
  17. Hobbach H. P., Hurth S., Jost D., Racké K. Effects of tetraethylammonium ions on frequency-dependent vasopressin release from the rat neurohypophysis. J Physiol. 1988 Mar;397:539–554. doi: 10.1113/jphysiol.1988.sp017018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lemos J. R., Nowycky M. C. Two types of calcium channels coexist in peptide-releasing vertebrate nerve terminals. Neuron. 1989 May;2(5):1419–1426. doi: 10.1016/0896-6273(89)90187-6. [DOI] [PubMed] [Google Scholar]
  19. Leng G., Shibuki K., Way S. A. Effects of raised extracellular potassium on the excitability of, and hormone release from, the isolated rat neurohypophysis. J Physiol. 1988 May;399:591–605. doi: 10.1113/jphysiol.1988.sp017098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mason W. T., Dyball R. E. Single ion channel activity in peptidergic nerve terminals of the isolated rat neurohypophysis related to stimulation of neural stalk axons. Brain Res. 1986 Sep 24;383(1-2):279–286. doi: 10.1016/0006-8993(86)90026-0. [DOI] [PubMed] [Google Scholar]
  21. Nagano M., Cooke I. M. Comparison of electrical responses of terminals, axons, and somata of a peptidergic neurosecretory system. J Neurosci. 1987 Mar;7(3):634–648. doi: 10.1523/JNEUROSCI.07-03-00634.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Negoro H., Visessuwan S., Holland R. C. Reflex activation of paraventricular nucleus units during the reproductive cycle and in ovariectomized rats treated with oestrogen or progesterone. J Endocrinol. 1973 Dec;59(3):559–567. doi: 10.1677/joe.0.0590559. [DOI] [PubMed] [Google Scholar]
  23. Nordmann J. J., Stuenkel E. L. Electrical properties of axons and neurohypophysial nerve terminals and their relationship to secretion in the rat. J Physiol. 1986 Nov;380:521–539. doi: 10.1113/jphysiol.1986.sp016300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nordmann J. J. Ultrastructural morphometry of the rat neurohypophysis. J Anat. 1977 Feb;123(Pt 1):213–218. [PMC free article] [PubMed] [Google Scholar]
  25. Obaid A. L., Orkand R. K., Gainer H., Salzberg B. M. Active calcium responses recorded optically from nerve terminals of the frog neurohypophysis. J Gen Physiol. 1985 Apr;85(4):481–489. doi: 10.1085/jgp.85.4.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pittman Q. J. Increases in antidromic latency of neurohypophyseal neurons during sustained activation. Neurosci Lett. 1983 Jun 30;37(3):239–243. doi: 10.1016/0304-3940(83)90437-8. [DOI] [PubMed] [Google Scholar]
  27. Poulain D. A., Wakerley J. B. Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience. 1982 Apr;7(4):773–808. doi: 10.1016/0306-4522(82)90044-6. [DOI] [PubMed] [Google Scholar]
  28. Salzberg B. M., Obaid A. L., Senseman D. M., Gainer H. Optical recording of action potentials from vertebrate nerve terminals using potentiometric probes provides evidence for sodium and calcium components. Nature. 1983 Nov 3;306(5938):36–40. doi: 10.1038/306036a0. [DOI] [PubMed] [Google Scholar]
  29. Summerlee A. J. Extracellular recordings from oxytocin neurones during the expulsive phase of birth in unanaesthetized rats. J Physiol. 1981 Dec;321:1–9. doi: 10.1113/jphysiol.1981.sp013967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wakerley J. B., Lincoln D. W. The milk-ejection reflex of the rat: a 20- to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release. J Endocrinol. 1973 Jun;57(3):477–493. doi: 10.1677/joe.0.0570477. [DOI] [PubMed] [Google Scholar]
  31. Wolfe S. A., Jr, Gainer H. Effects of calcium on frequency-modulated secretion of vasopressin from isolated murine neural lobes. Brain Res. 1986 Dec 3;399(1):190–193. doi: 10.1016/0006-8993(86)90618-9. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES