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Magnocellular Neurons and Posterior Pituitary Function

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ABSTRACT

The posterior pituitary gland secretes oxytocin and vasopressin (the antidiuretic hormone) into the blood system. Oxytocin is required for normal delivery of the young and for delivery of milk to the young during lactation. Vasopressin increases water reabsorption in the kidney to maintain body fluid balance and causes vasoconstriction to increase blood pressure. Oxytocin and vasopressin secretion occurs from the axon terminals of magnocellular neurons whose cell bodies are principally found in the hypothalamic supraoptic nucleus and paraventricular nucleus. The physiological functions of oxytocin and vasopressin depend on their secretion, which is principally determined by the pattern of action potentials initiated at the cell bodies. Appropriate secretion of oxytocin and vasopressin to meet the challenges of changing physiological conditions relies mainly on integration of afferent information on reproductive, osmotic, and cardiovascular status with local regulation of magnocellular neurons by glia as well as intrinsic regulation by the magnocellular neurons themselves. This review focuses on the control of magnocellular neuron activity with a particular emphasis on their regulation by reproductive function, body fluid balance, and cardiovascular status. © 2016 American Physiological Society. Compr Physiol 6:1701‐1741, 2016.

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Figure 1. Figure 1. The magnocellular neurosecretory system. (A‐C) Photomicrographs of coronal sections of rat hypothalamus (A), in which oxytocin neurons are immunostained with fluorescent red and vasopressin neurons with fluorescent green. Magnocellular neuron cell bodies are principally found in the hypothalamic SON (B), lateral to the optic chiasm (OC), and PVN (C), lateral to the third cerebral ventricle (3V). The SON contains only magnocellular neurons that project to the posterior pituitary gland, whereas the PVN also contains parvocellular oxytocin and vasopressin neurons (as well as other parvocellular neurons) that project elsewhere in the brain. (D) Photomicrograph of vasopressin axon terminals in the posterior pituitary gland. (E) Electron micrograph showing magnocellular neuron dendrites densely packed with dense‐core vesicles (small black dots). Reproduced, with permission, from ().
Figure 2. Figure 2. Schematic representation of some of the major peripheral and afferent inputs to magnocellular neurosecretory cells. See text for details of the physiological functions of each of the inputs. Abbreviations: ARN: arcuate nucleus; BNST: bed nucleus of the stria terminalis; DBB: diagonal band of Broca; DRN: dorsal raphe nucleus; LC: locus coeruleus; MNC: magnocellular neurosecretory cell (magnocellular neuron); MnPO: median preoptic nucleus; MRN: median raphe nucleus; NTS: nucleus tractus solitarius; OB: olfactory bulb; OVLT: organum vasculosum of the lamina terminalis; pcSN: pars compacta of the substantia nigra; PNZ: perinuclear zone; PPAH: preoptic periventricular /anterior hypothalamic region; SCN: suprachiasmatic nucleus; SFO: subfornical organ; TM: tuberomammillary nucleus; VLM: ventrolateral medulla; VTA: ventral tegmental area. Reproduced, with permission, from ().
Figure 3. Figure 3. Frequency facilitation of oxytocin and vasopressin release from the posterior pituitary gland. Isolated posterior pituitary glands were electrically stimulated with 156 pulses delivered at each of the four frequencies indicated in a balanced order of presentation. Evoked hormone release is expressed as a percentage of the total release evoked by the four stimulations. Note that hormone release is facilitated at higher frequencies, that little hormone is released at frequencies of <4 Hz and that frequency facilitation of vasopressin release peaks at a lower frequency than for oxytocin release. Modified, with permission, from ().
Figure 4. Figure 4. Activity patterning in oxytocin and vasopressin neurons. Each panel shows a typical example ratemeter record (in 1 s bins) of the various spontaneous activity patterns of oxytocin and vasopressin neurons recorded from urethane‐anesthetized rats (excluding silent neurons). (A and B) Irregular activity; note that the overall firing rates of the two neurons are similar (at ∼2.5 spikes s−1), but the variability of firing rate is lower for the oxytocin neuron in (A) than for the vasopressin neuron in (B). (C and D) Continuous activity; note that the overall firing rate of the oxytocin neuron in C (at ∼4 spikes s−1) is lower than the vasopressin neuron in D (at ∼6 spikes s−1). (E) Milk ejection bursts from an oxytocin neuron in a urethane‐anesthetized rat being suckled during lactation; note the short, high‐frequency milk‐ejection bursts that occur every few minutes, and are followed by short periods of silence. Because milk ejection bursts are coordinated across the population of oxytocin neurons, each burst releases a pulse of oxytocin that increases intramammary pressure (insets). Data kindly provided by Prof J. A. Russell, University of Edinburgh. F, Phasic activity from a vasopressin neuron; note the periods of activity that last for tens of seconds (phasic bursts) that are followed by periods of silence that also last for tens of seconds as well as the spike frequency adaptation from the initial high firing rate to a steady‐state firing rate during each burst.
Figure 5. Figure 5. Postspike potentials and phasic firing. All panels show a sharp electrode intracellular recording of membrane potential in a magnocellular neuron. (A) A single action potential with an associated fast afterhyperpolarization (fAHP) in a vasopressin neuron. (B) A train of five evoked spikes (arrowhead, truncated) and an associated summated medium afterhyperpolarization (mAHP) in an oxytocin neuron. (C) A train of 25 evoked spikes (arrowhead, truncated) and an associated summated slow afterhyperpolarization (sAHP) in a vasopressin neuron. (D) A train of five evoked spikes (arrowhead, truncated) and an associated summated mAHP and slow afterdepolarization (sADP) in a vasopressin neuron. (E) A train of five evoked spikes (arrowhead, truncated) recorded in the presence of 1 μmol/L apamin to block the mAHP and thereby expose the fast ADP (fADP), along with the sADP, in a vasopressin neuron. (F) The middle panel shows a sequence of three spontaneous phasic bursts. The left‐hand inset shows the onset of a spontaneous burst, with summation of sADPs to generate a plateau potential. The right‐hand inset shows the final spike (arrowhead, truncated) averaged from 21 spontaneous bursts (filtered) with the associated postburst sADP and sAHP.
Figure 6. Figure 6. Postspike potentials underpin postspike excitability in magnocellular neurosecretory cells. (A and B) Schematic representations of individual spikes, postspike potentials, and excitatory synaptic potentials (EPSPs) (not to scale) from (A) an oxytocin neuron and (B) a vasopressin neuron. All magnocellular neurons exhibit a prominent postspike mAHP that initially hyperpolarizes the neuron after each spike, reducing the probability that ongoing EPSPs will reach spike threshold. Vasopressin neurons also exhibit a prominent postspike sADP (that is lower amplitude and longer lasting than the mAHP and so becomes evident when the mAHP is decaying); the sADP depolarizes the neuron for a relatively long period, increasing the probability that summation of ongoing EPSPs will reach spike threshold and trigger a further spike. If, as shown, a further spike does not fire, the membrane potential returns to baseline. (C and D) Schematic representations of interspike interval histograms constructed from spike firing of (C) an oxytocin neuron and (D) a vasopressin neuron. Very short intervals are rare, reflecting the inhibitory influence of the mAHP (as well as other hyperpolarizing postspike potentials). The tails of both histograms are fit by single exponential decays (dashed lines); for vasopressin neurons, but not oxytocin neurons, the single exponential does not fit the peak of the histogram and the excess short intervals reflect the excitatory influence of the sADP. (E and F) Schematic representations of hazard functions for (E) an oxytocin neuron and (F) a vasopressin neuron. Hazard functions show the probability of the next spike firing with time after the preceding spike and represent the postspike excitability of neurons. The postspike refractoriness reflects the inhibitory influence of the mAHP and the postspike hyperexcitability reflects the excitatory influence of the sADP. Hazards are calculated from the interspike histograms using the formula: h[i‐1, i] = n[i‐1, 1]/(Nn[0, i‐1]), where h[i‐1, i] is the hazard at interspike interval i, n[i‐1, 1] is the number of spikes in interspike interval i, n[0, i‐1] is the total number of spikes preceding the current interspike interval and N is the total number of spikes in all interspike intervals.
Figure 7. Figure 7. Autocrine modulation of phasic activity. Schematic representation of the mechanisms of autocrine modulation of phasic activity by vasopressin, adenosine and dynorphin. Activity‐dependent somatodendritic release of vasopressin causes an immediate inhibition of EPSP amplitude that causes a tonic suppression of activity; ATP is secreted with vasopressin and is rapidly converted to adenosine, which enhances the mAHP to increase spike frequency adaptation over the first few second of the burst; dynorphin is also secreted with vasopressin and progressively increases inhibition of the sADP over tens of seconds to, eventually, lead to burst termination.
Figure 8. Figure 8. Lack of coordination of phasic bursts. Ratemeter records of the spontaneous activity (averaged in 1 s bins) of two phasic vasopressin neurons that were simultaneously recorded from the supraoptic nucleus of a urethane‐anesthetized rat. Note the absence of coordination between the onset and termination of bursts between the two neurons.
Figure 9. Figure 9. Coordination of milk‐ejection bursts. Ratemeter records of the spontaneous activity (averaged in 1 s bins) of two oxytocin neurons that were simultaneously recorded from the supraoptic nucleus of a urethane‐anesthetized lactating rat with suckling pups. Note the coordination between timing of bursts between the two neurons.
Figure 10. Figure 10. Priming somatodendritic oxytocin release. (A) Calcium influx triggers somatodendritic oxytocin release. (B) Oxytocin activates oxytocin receptors on the plasma membrane to increase intracellular IP3 concentrations. (C) IP3 increases calcium release from the endoplasmic reticulum to (D) mobilize dense‐core vesicles from the reserve pool to the readily releasable pool, “priming” magnocellular neurons to release increased amounts of oxytocin in response to subsequent stimuli. Reproduced, with permission, from ().
Figure 11. Figure 11. Glial regulation of magnocellular neuron activity under basal conditions. (A) α1‐Adrenoreceptor (αAR) or groups 1 and 5 metabotropic glutamate receptor (mGluR) activation increases intracellular calcium in astrocytes via inositol triphosphate (IP3) to trigger ATP release. ATP activates magnocellular neuron P2X receptors (P2XR) to increase calcium influx, which activates phosphotidyl inositol 3‐kinase (PI3K) to increase AMPA receptor (AMPAR) insertion into the postsynaptic membrane, mediating long‐term potentiation of glutamate synapses (synaptic scaling). (B) Astrocyte glutamate transporters (GLT‐1) remove glutamate from the extracellular space to limit activation of extrasynaptic NMDA receptors (eNMDAR). (C) Astrocytes release D‐serine to act as a coagonist with glutamate at postsynaptic NMDARs on magnocellular neurons. (D) Astrocytes release taurine through volume‐regulated anion channels (VRA) to activate extrasynaptic glycine receptors (GlyR) to hyperpolarize the magnocellular neuron via chloride influx. Reproduced, with permission, from ().


Figure 1. The magnocellular neurosecretory system. (A‐C) Photomicrographs of coronal sections of rat hypothalamus (A), in which oxytocin neurons are immunostained with fluorescent red and vasopressin neurons with fluorescent green. Magnocellular neuron cell bodies are principally found in the hypothalamic SON (B), lateral to the optic chiasm (OC), and PVN (C), lateral to the third cerebral ventricle (3V). The SON contains only magnocellular neurons that project to the posterior pituitary gland, whereas the PVN also contains parvocellular oxytocin and vasopressin neurons (as well as other parvocellular neurons) that project elsewhere in the brain. (D) Photomicrograph of vasopressin axon terminals in the posterior pituitary gland. (E) Electron micrograph showing magnocellular neuron dendrites densely packed with dense‐core vesicles (small black dots). Reproduced, with permission, from ().


Figure 2. Schematic representation of some of the major peripheral and afferent inputs to magnocellular neurosecretory cells. See text for details of the physiological functions of each of the inputs. Abbreviations: ARN: arcuate nucleus; BNST: bed nucleus of the stria terminalis; DBB: diagonal band of Broca; DRN: dorsal raphe nucleus; LC: locus coeruleus; MNC: magnocellular neurosecretory cell (magnocellular neuron); MnPO: median preoptic nucleus; MRN: median raphe nucleus; NTS: nucleus tractus solitarius; OB: olfactory bulb; OVLT: organum vasculosum of the lamina terminalis; pcSN: pars compacta of the substantia nigra; PNZ: perinuclear zone; PPAH: preoptic periventricular /anterior hypothalamic region; SCN: suprachiasmatic nucleus; SFO: subfornical organ; TM: tuberomammillary nucleus; VLM: ventrolateral medulla; VTA: ventral tegmental area. Reproduced, with permission, from ().


Figure 3. Frequency facilitation of oxytocin and vasopressin release from the posterior pituitary gland. Isolated posterior pituitary glands were electrically stimulated with 156 pulses delivered at each of the four frequencies indicated in a balanced order of presentation. Evoked hormone release is expressed as a percentage of the total release evoked by the four stimulations. Note that hormone release is facilitated at higher frequencies, that little hormone is released at frequencies of <4 Hz and that frequency facilitation of vasopressin release peaks at a lower frequency than for oxytocin release. Modified, with permission, from ().


Figure 4. Activity patterning in oxytocin and vasopressin neurons. Each panel shows a typical example ratemeter record (in 1 s bins) of the various spontaneous activity patterns of oxytocin and vasopressin neurons recorded from urethane‐anesthetized rats (excluding silent neurons). (A and B) Irregular activity; note that the overall firing rates of the two neurons are similar (at ∼2.5 spikes s−1), but the variability of firing rate is lower for the oxytocin neuron in (A) than for the vasopressin neuron in (B). (C and D) Continuous activity; note that the overall firing rate of the oxytocin neuron in C (at ∼4 spikes s−1) is lower than the vasopressin neuron in D (at ∼6 spikes s−1). (E) Milk ejection bursts from an oxytocin neuron in a urethane‐anesthetized rat being suckled during lactation; note the short, high‐frequency milk‐ejection bursts that occur every few minutes, and are followed by short periods of silence. Because milk ejection bursts are coordinated across the population of oxytocin neurons, each burst releases a pulse of oxytocin that increases intramammary pressure (insets). Data kindly provided by Prof J. A. Russell, University of Edinburgh. F, Phasic activity from a vasopressin neuron; note the periods of activity that last for tens of seconds (phasic bursts) that are followed by periods of silence that also last for tens of seconds as well as the spike frequency adaptation from the initial high firing rate to a steady‐state firing rate during each burst.


Figure 5. Postspike potentials and phasic firing. All panels show a sharp electrode intracellular recording of membrane potential in a magnocellular neuron. (A) A single action potential with an associated fast afterhyperpolarization (fAHP) in a vasopressin neuron. (B) A train of five evoked spikes (arrowhead, truncated) and an associated summated medium afterhyperpolarization (mAHP) in an oxytocin neuron. (C) A train of 25 evoked spikes (arrowhead, truncated) and an associated summated slow afterhyperpolarization (sAHP) in a vasopressin neuron. (D) A train of five evoked spikes (arrowhead, truncated) and an associated summated mAHP and slow afterdepolarization (sADP) in a vasopressin neuron. (E) A train of five evoked spikes (arrowhead, truncated) recorded in the presence of 1 μmol/L apamin to block the mAHP and thereby expose the fast ADP (fADP), along with the sADP, in a vasopressin neuron. (F) The middle panel shows a sequence of three spontaneous phasic bursts. The left‐hand inset shows the onset of a spontaneous burst, with summation of sADPs to generate a plateau potential. The right‐hand inset shows the final spike (arrowhead, truncated) averaged from 21 spontaneous bursts (filtered) with the associated postburst sADP and sAHP.


Figure 6. Postspike potentials underpin postspike excitability in magnocellular neurosecretory cells. (A and B) Schematic representations of individual spikes, postspike potentials, and excitatory synaptic potentials (EPSPs) (not to scale) from (A) an oxytocin neuron and (B) a vasopressin neuron. All magnocellular neurons exhibit a prominent postspike mAHP that initially hyperpolarizes the neuron after each spike, reducing the probability that ongoing EPSPs will reach spike threshold. Vasopressin neurons also exhibit a prominent postspike sADP (that is lower amplitude and longer lasting than the mAHP and so becomes evident when the mAHP is decaying); the sADP depolarizes the neuron for a relatively long period, increasing the probability that summation of ongoing EPSPs will reach spike threshold and trigger a further spike. If, as shown, a further spike does not fire, the membrane potential returns to baseline. (C and D) Schematic representations of interspike interval histograms constructed from spike firing of (C) an oxytocin neuron and (D) a vasopressin neuron. Very short intervals are rare, reflecting the inhibitory influence of the mAHP (as well as other hyperpolarizing postspike potentials). The tails of both histograms are fit by single exponential decays (dashed lines); for vasopressin neurons, but not oxytocin neurons, the single exponential does not fit the peak of the histogram and the excess short intervals reflect the excitatory influence of the sADP. (E and F) Schematic representations of hazard functions for (E) an oxytocin neuron and (F) a vasopressin neuron. Hazard functions show the probability of the next spike firing with time after the preceding spike and represent the postspike excitability of neurons. The postspike refractoriness reflects the inhibitory influence of the mAHP and the postspike hyperexcitability reflects the excitatory influence of the sADP. Hazards are calculated from the interspike histograms using the formula: h[i‐1, i] = n[i‐1, 1]/(Nn[0, i‐1]), where h[i‐1, i] is the hazard at interspike interval i, n[i‐1, 1] is the number of spikes in interspike interval i, n[0, i‐1] is the total number of spikes preceding the current interspike interval and N is the total number of spikes in all interspike intervals.


Figure 7. Autocrine modulation of phasic activity. Schematic representation of the mechanisms of autocrine modulation of phasic activity by vasopressin, adenosine and dynorphin. Activity‐dependent somatodendritic release of vasopressin causes an immediate inhibition of EPSP amplitude that causes a tonic suppression of activity; ATP is secreted with vasopressin and is rapidly converted to adenosine, which enhances the mAHP to increase spike frequency adaptation over the first few second of the burst; dynorphin is also secreted with vasopressin and progressively increases inhibition of the sADP over tens of seconds to, eventually, lead to burst termination.


Figure 8. Lack of coordination of phasic bursts. Ratemeter records of the spontaneous activity (averaged in 1 s bins) of two phasic vasopressin neurons that were simultaneously recorded from the supraoptic nucleus of a urethane‐anesthetized rat. Note the absence of coordination between the onset and termination of bursts between the two neurons.


Figure 9. Coordination of milk‐ejection bursts. Ratemeter records of the spontaneous activity (averaged in 1 s bins) of two oxytocin neurons that were simultaneously recorded from the supraoptic nucleus of a urethane‐anesthetized lactating rat with suckling pups. Note the coordination between timing of bursts between the two neurons.


Figure 10. Priming somatodendritic oxytocin release. (A) Calcium influx triggers somatodendritic oxytocin release. (B) Oxytocin activates oxytocin receptors on the plasma membrane to increase intracellular IP3 concentrations. (C) IP3 increases calcium release from the endoplasmic reticulum to (D) mobilize dense‐core vesicles from the reserve pool to the readily releasable pool, “priming” magnocellular neurons to release increased amounts of oxytocin in response to subsequent stimuli. Reproduced, with permission, from ().


Figure 11. Glial regulation of magnocellular neuron activity under basal conditions. (A) α1‐Adrenoreceptor (αAR) or groups 1 and 5 metabotropic glutamate receptor (mGluR) activation increases intracellular calcium in astrocytes via inositol triphosphate (IP3) to trigger ATP release. ATP activates magnocellular neuron P2X receptors (P2XR) to increase calcium influx, which activates phosphotidyl inositol 3‐kinase (PI3K) to increase AMPA receptor (AMPAR) insertion into the postsynaptic membrane, mediating long‐term potentiation of glutamate synapses (synaptic scaling). (B) Astrocyte glutamate transporters (GLT‐1) remove glutamate from the extracellular space to limit activation of extrasynaptic NMDA receptors (eNMDAR). (C) Astrocytes release D‐serine to act as a coagonist with glutamate at postsynaptic NMDARs on magnocellular neurons. (D) Astrocytes release taurine through volume‐regulated anion channels (VRA) to activate extrasynaptic glycine receptors (GlyR) to hyperpolarize the magnocellular neuron via chloride influx. Reproduced, with permission, from ().
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Further Reading List

Bourque CW. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 9: 519-531, 2008.

Brown CH, Bains JS, Ludwig M, and Stern JE. Physiological regulation of magnocellular neurosecretory cell activity: Integration of intrinsic, local and afferent mechanisms. J Neuroendocrinol 25: 678-710, 2013.

Brunton PJ and Russell JA. The expectant brain: adapting for motherhood. Nat Rev Neurosci 9: 11-25, 2008.

Tasker JG, Oliet SH, Bains JS, Brown CH, and Stern JE. Glial regulation of neuronal function: from synapse to systems physiology. J Neuroendocrinol 24: 566-576, 2012.

 


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Colin H. Brown. Magnocellular Neurons and Posterior Pituitary Function. Compr Physiol 2016, 6: 1701-1741. doi: 10.1002/cphy.c150053