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Cellular Biology of the Neurosecretory Neuron

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Abstract

The sections in this article are:

1 Cytology of Neurosecretory Neurons
2 Neurosecretory Granules
3 Synthesis of Neurosecretion
4 Axonal Transport of Neurosecretory Material
4.1 Phenomenon of Transport
4.2 Rates of Transport
4.3 Effect of Electrical Activity on Transport
4.4 Mechanism of Transport
4.5 Modification of Neurosecretion During Transport
5 Release of Neurosecretory Material
6 Intraneuronal Carrier Proteins
7 Electrophysiology of Neurosecretory Neurons
8 Synaptology
9 Relations with Glial Elements
10 Regeneration of Neurosecretory Neurons
11 Addendum
Figure 1. Figure 1.

Neuronal structure of protocerebral medial neurosecretory neuron from cockroach (left) as compared with generalized invertebrate neuron (right); a, axon; co, collaterals; d, dendrite; nsm, neurosecretory material; pe, perikaryon; te, axon terminals.

From Adiyodi & Bern
Figure 2. Figure 2.

Neurosecretory granules in axon terminals of the rat neurohypophysis. Tissue was fixed in triple‐aldehyde fixative at pH 5, 6,7, and 8. Note decreasing density of granule contents with increasing pH and rupture of granules at pH 8. × 21,659.

From J. F. Morris, unpublished
Figure 3. Figure 3.

Ultra‐autoradiographs of supraoptic neurons of rat injected intracisternally with [3H]cysteine 5 min (A) and 1 h (B) before sacrifice. Note silver grains over endoplasmic reticulum in A and over Golgi zones in B.

From R. S. Nishioka, D. Zambrano, and H. A. Bern, unpublished; cf.
Figure 4. Figure 4.

Axon from proximal stump of transected frog hypothalamoneurohypophysial tract 12 h after transection to show tubular formations and their connections with neurosecretory granules, × 27,000.

From H.‐D. Dellmann and E. M. Rodriguez, unpublished; cf.
Figure 5. Figure 5.

Polygraph recordings to illustrate acceleration in the activity of a supraoptic neuron (SO) in a rat that immediately precedes oxytocin release. Each vertical deflection on the unit trace corresponds to a single action potential; the amplitude of the integration trace corresponds to frequency; 10 rat pups were suckling throughout. Note that the rise in intramammary pressure, which represents milk ejection, occurs 12–14 s after the activation of the supraoptic cell and the subsequent pulse of oxytocin.

From D. W. Lincoln, unpublished
Figure 6. Figure 6.

Relationship between electrical activity of neurosecretory cells and release of oxytocin in rats. Number of supraoptic (SO) and paraventricular (PV) neurons and the oxytocin content of the neurohypophysis are given in the center of the figure. Total spike traffic in the hypothalamoneurohypophysial tract is compared with the basal release of oxytocin (left) and the pulsatile release of oxytocin during suckling (right). In the latter calculation, the contribution to spike activity of the 9,000 unresponsive SO and PV cells has been ignored. Note the 100‐fold facilitation in the amount of hormone released per spike in the burst of activity that causes milk ejection.

From Lincoln
Figure 7. Figure 7.

Electron micrographs from neural lobe presenting evidence for exocytosis of elementary neurosecretory granules (A and B) and formation of small vesicles by pinocytosis (C; D with arrow). A, rat. × 78,000. B, hamster (“omega figure”), × 94,000. C, hamster, × 17,000. D, hamster, × 78,000

A and B from Nagasawa et al. ; C and D from Douglas et al.
Figure 8. Figure 8.

Postulated sequence of events in exocytosis of granules from neurosecretory axon terminal and in recapture of granule membrane leading to formation of small vesicles.

Based on the studies of W. W. Douglas and his collaborators
Figure 9. Figure 9.

Recordings from neurosecretory neurons. A: intracellular spontaneous spike from neurosecretory soma of cockroach pars intercerebralis; note conspicuous hyperpolarizing afterpotential. B: intracellular evoked spike from intrinsic cell soma of blowfly corpus cardiacum. C: intracellular directly evoked spike from neurosecretory soma of crayfish X organ. D: intracellular antidromically evoked spike from neurosecretory soma of crayfish X organ. E and F: difference in the active components of action potentials between soma and axon in crayfish X organ neurosecretory system. In the normal medium (E) the action potential of the soma (upper) elicited by a direct current injected in the neuron soma and the corresponding spike potential of the axon (lower) were seen as a one‐to‐one relationship. A spontaneous spike potential of another neuron is also seen (asterisk). After application of tetrodotoxin (F) the spike potentials of the axon disappeared, while the spike potential of the neuron soma remained. G: antidromically evoked spike from rat supraoptic neuron. H: antidromically evoked spike from cat or dog supraoptic or paraventricular neuron to show small spike (inflection in rising phase) presumably originating from the axon hillock region and large spike presumably somatodendritic in origin. I: intracellular action potential from ordinary neuron in eel posterior spinal cord stimulated by directly applied outward current. J: intracellular action potential from eel caudal neurosecretory neuron stimulated by intracellularly applied 5‐ms depolarizing current. In A‐J, horizontal line in milliseconds, vertical line in millivolts

A from Cook & Milligan ; B from Normann ; C‐F from Iwasaki & Satow ; G from Yagi et al. ; H from Koizumi & Yamashita ; I and J from Ishibashi
Figure 10. Figure 10.

Synapses onto neurosecretory cells of the paraventricular nucleus of the rat. A: process extending from a cell body, × 12,500. B: isolated process in the paraventricular region, × 14,700. Both elements contain neurosecretory granules (ng) and display typical synaptic contacts (s), but in neither case is it possible to be certain whether the profiles are axons as opposed to dendrites. Further the process in A lacks the characteristic features of an axon hillock, and such features are not seen in processes extending from neurosecretory cell bodies in the rat hypothalamus. The pale appearance of granules in both A and B is due to long fixation (i.e., overnight) at pH 7.3.

From J. F. Morris, unpublished
Figure 11. Figure 11.

A: pars nervosa of white‐crowned sparrow. Glial elements (G) interposed between axon endings (containing many small vesicles and dense granules) and basement membrane (BM) of capillary. B: supraesophageal ganglion of leech (Theromyzon rude). Neurosecretory cell (granule‐filled) with processes (P) from glial cell (G) invaginating into cytoplasm is shown. N, glial nucleus. [From R. S. Nishioka and I. R. Hagadorn, unpublished; cf. .]

From R. S. Nishioka and H. A. Bern, unpublished; cf.


Figure 1.

Neuronal structure of protocerebral medial neurosecretory neuron from cockroach (left) as compared with generalized invertebrate neuron (right); a, axon; co, collaterals; d, dendrite; nsm, neurosecretory material; pe, perikaryon; te, axon terminals.

From Adiyodi & Bern


Figure 2.

Neurosecretory granules in axon terminals of the rat neurohypophysis. Tissue was fixed in triple‐aldehyde fixative at pH 5, 6,7, and 8. Note decreasing density of granule contents with increasing pH and rupture of granules at pH 8. × 21,659.

From J. F. Morris, unpublished


Figure 3.

Ultra‐autoradiographs of supraoptic neurons of rat injected intracisternally with [3H]cysteine 5 min (A) and 1 h (B) before sacrifice. Note silver grains over endoplasmic reticulum in A and over Golgi zones in B.

From R. S. Nishioka, D. Zambrano, and H. A. Bern, unpublished; cf.


Figure 4.

Axon from proximal stump of transected frog hypothalamoneurohypophysial tract 12 h after transection to show tubular formations and their connections with neurosecretory granules, × 27,000.

From H.‐D. Dellmann and E. M. Rodriguez, unpublished; cf.


Figure 5.

Polygraph recordings to illustrate acceleration in the activity of a supraoptic neuron (SO) in a rat that immediately precedes oxytocin release. Each vertical deflection on the unit trace corresponds to a single action potential; the amplitude of the integration trace corresponds to frequency; 10 rat pups were suckling throughout. Note that the rise in intramammary pressure, which represents milk ejection, occurs 12–14 s after the activation of the supraoptic cell and the subsequent pulse of oxytocin.

From D. W. Lincoln, unpublished


Figure 6.

Relationship between electrical activity of neurosecretory cells and release of oxytocin in rats. Number of supraoptic (SO) and paraventricular (PV) neurons and the oxytocin content of the neurohypophysis are given in the center of the figure. Total spike traffic in the hypothalamoneurohypophysial tract is compared with the basal release of oxytocin (left) and the pulsatile release of oxytocin during suckling (right). In the latter calculation, the contribution to spike activity of the 9,000 unresponsive SO and PV cells has been ignored. Note the 100‐fold facilitation in the amount of hormone released per spike in the burst of activity that causes milk ejection.

From Lincoln


Figure 7.

Electron micrographs from neural lobe presenting evidence for exocytosis of elementary neurosecretory granules (A and B) and formation of small vesicles by pinocytosis (C; D with arrow). A, rat. × 78,000. B, hamster (“omega figure”), × 94,000. C, hamster, × 17,000. D, hamster, × 78,000

A and B from Nagasawa et al. ; C and D from Douglas et al.


Figure 8.

Postulated sequence of events in exocytosis of granules from neurosecretory axon terminal and in recapture of granule membrane leading to formation of small vesicles.

Based on the studies of W. W. Douglas and his collaborators


Figure 9.

Recordings from neurosecretory neurons. A: intracellular spontaneous spike from neurosecretory soma of cockroach pars intercerebralis; note conspicuous hyperpolarizing afterpotential. B: intracellular evoked spike from intrinsic cell soma of blowfly corpus cardiacum. C: intracellular directly evoked spike from neurosecretory soma of crayfish X organ. D: intracellular antidromically evoked spike from neurosecretory soma of crayfish X organ. E and F: difference in the active components of action potentials between soma and axon in crayfish X organ neurosecretory system. In the normal medium (E) the action potential of the soma (upper) elicited by a direct current injected in the neuron soma and the corresponding spike potential of the axon (lower) were seen as a one‐to‐one relationship. A spontaneous spike potential of another neuron is also seen (asterisk). After application of tetrodotoxin (F) the spike potentials of the axon disappeared, while the spike potential of the neuron soma remained. G: antidromically evoked spike from rat supraoptic neuron. H: antidromically evoked spike from cat or dog supraoptic or paraventricular neuron to show small spike (inflection in rising phase) presumably originating from the axon hillock region and large spike presumably somatodendritic in origin. I: intracellular action potential from ordinary neuron in eel posterior spinal cord stimulated by directly applied outward current. J: intracellular action potential from eel caudal neurosecretory neuron stimulated by intracellularly applied 5‐ms depolarizing current. In A‐J, horizontal line in milliseconds, vertical line in millivolts

A from Cook & Milligan ; B from Normann ; C‐F from Iwasaki & Satow ; G from Yagi et al. ; H from Koizumi & Yamashita ; I and J from Ishibashi


Figure 10.

Synapses onto neurosecretory cells of the paraventricular nucleus of the rat. A: process extending from a cell body, × 12,500. B: isolated process in the paraventricular region, × 14,700. Both elements contain neurosecretory granules (ng) and display typical synaptic contacts (s), but in neither case is it possible to be certain whether the profiles are axons as opposed to dendrites. Further the process in A lacks the characteristic features of an axon hillock, and such features are not seen in processes extending from neurosecretory cell bodies in the rat hypothalamus. The pale appearance of granules in both A and B is due to long fixation (i.e., overnight) at pH 7.3.

From J. F. Morris, unpublished


Figure 11.

A: pars nervosa of white‐crowned sparrow. Glial elements (G) interposed between axon endings (containing many small vesicles and dense granules) and basement membrane (BM) of capillary. B: supraesophageal ganglion of leech (Theromyzon rude). Neurosecretory cell (granule‐filled) with processes (P) from glial cell (G) invaginating into cytoplasm is shown. N, glial nucleus. [From R. S. Nishioka and I. R. Hagadorn, unpublished; cf. .]

From R. S. Nishioka and H. A. Bern, unpublished; cf.
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Carol Ann Mason, Howard A. Bern. Cellular Biology of the Neurosecretory Neuron. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 651-689. First published in print 1977. doi: 10.1002/cphy.cp010118