Elevated extracellular potassium is associated with a reduced extracellular space in rat neural lobe in vitro

William Armstrong, M. Tian, J. F. Reger

Research output: Contribution to journalArticle

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Abstract

Increased neural activity of neurosecretory cells is accompanied by large increases in extracellular K+. The possibility that elevations of this ion might involve fluid redistribution and thus affect the size of the extracellular space and the relationship between pituicytes and axons in the rat neural lobe was explored using rapid freezing and freeze-substitution. Neural lobes were incubated for 15 min before freezing either in a normal medium or one containing a 10 mM increase in KCl (high KCl), a 10 mM increase in KCl balanced by an equimolar reduction in NaCl (high KCl-low NaCl), or only a 10 mM reduction in NaCl (low NaCl). A quantitative assessment of the region of good fixation was made to determine the relative fractions occupied by axons, pituicytes and the extracellular space near the neurohaemal contact zone. In addition, the percentage of basal lamina contacted by pituicytes and axons was calculated, as was the degree of enclosure of axons by pituicytes. In neural lobes incubated in normal medium, the extracellular space accounted for approximately 30% of the cross-sectional area of the neuropil and could be divided into two domains: an extended perivascular space (28-29% of total area); and a narrow (approximately 24 nm; approximately 1% of total) space between closely apposed neurosecretory processes or between these processes and pituicytes. Pituicytes occupied almost 60% of the basal lamina at the neurohaemal contact zone, while axons occupied approximately 20%. Neural lobes incubated in either the high KCl solution, or in the high KCl-low NaCl solution, exhibited a significantly reduced extracellular space, to about 20% of the total area, or a reduction from controls of about one-third. The reduction was complemented by an increased area occupied by axons plus pituicytes. In the high KCl group, the contribution of the narrow spaces (22-24 nm) between apposed processes to the total extracellular space was greatly increased. The group exposed to low NaCl showed high variability in the size of extracellular space, and was thus not significantly different from any other group. No changes in any group were observed in the enclosure of axons by pituicytes, or in the relative amounts of axon and pituicyte apposition to the basal lamina. The subsequent buffering of K+ and other ions during periods of increased neuronal activity may be affected by changes in the extracellular space, thereby influencing stimulus-secretion coupling. A shrinkage of the extracellular space and the relative increase in the narrow spaces between processes initiated by elevated K+ could also alter the diffusion properties of the neural lobe.

Original languageEnglish (US)
Pages (from-to)564-572
Number of pages9
JournalJournal of Neurocytology
Volume20
Issue number7
DOIs
StatePublished - Jul 1 1991

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Posterior Pituitary Gland
Extracellular Space
Axons
Potassium
Basement Membrane
Freezing
Freeze Substitution
Ions
Neuropil
In Vitro Techniques

All Science Journal Classification (ASJC) codes

  • Anatomy
  • Neuroscience(all)
  • Histology
  • Cell Biology

Cite this

Elevated extracellular potassium is associated with a reduced extracellular space in rat neural lobe in vitro. / Armstrong, William; Tian, M.; Reger, J. F.

In: Journal of Neurocytology, Vol. 20, No. 7, 01.07.1991, p. 564-572.

Research output: Contribution to journalArticle

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abstract = "Increased neural activity of neurosecretory cells is accompanied by large increases in extracellular K+. The possibility that elevations of this ion might involve fluid redistribution and thus affect the size of the extracellular space and the relationship between pituicytes and axons in the rat neural lobe was explored using rapid freezing and freeze-substitution. Neural lobes were incubated for 15 min before freezing either in a normal medium or one containing a 10 mM increase in KCl (high KCl), a 10 mM increase in KCl balanced by an equimolar reduction in NaCl (high KCl-low NaCl), or only a 10 mM reduction in NaCl (low NaCl). A quantitative assessment of the region of good fixation was made to determine the relative fractions occupied by axons, pituicytes and the extracellular space near the neurohaemal contact zone. In addition, the percentage of basal lamina contacted by pituicytes and axons was calculated, as was the degree of enclosure of axons by pituicytes. In neural lobes incubated in normal medium, the extracellular space accounted for approximately 30{\%} of the cross-sectional area of the neuropil and could be divided into two domains: an extended perivascular space (28-29{\%} of total area); and a narrow (approximately 24 nm; approximately 1{\%} of total) space between closely apposed neurosecretory processes or between these processes and pituicytes. Pituicytes occupied almost 60{\%} of the basal lamina at the neurohaemal contact zone, while axons occupied approximately 20{\%}. Neural lobes incubated in either the high KCl solution, or in the high KCl-low NaCl solution, exhibited a significantly reduced extracellular space, to about 20{\%} of the total area, or a reduction from controls of about one-third. The reduction was complemented by an increased area occupied by axons plus pituicytes. In the high KCl group, the contribution of the narrow spaces (22-24 nm) between apposed processes to the total extracellular space was greatly increased. The group exposed to low NaCl showed high variability in the size of extracellular space, and was thus not significantly different from any other group. No changes in any group were observed in the enclosure of axons by pituicytes, or in the relative amounts of axon and pituicyte apposition to the basal lamina. The subsequent buffering of K+ and other ions during periods of increased neuronal activity may be affected by changes in the extracellular space, thereby influencing stimulus-secretion coupling. A shrinkage of the extracellular space and the relative increase in the narrow spaces between processes initiated by elevated K+ could also alter the diffusion properties of the neural lobe.",
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