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Endocrine‐Autonomic Linkages

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ABSTRACT

Interaction between the autonomic nervous system and the neuroendocrine system is critical for maintenance of homeostasis in a wide variety of physiological parameters such as body temperature, fluid and electrolyte balance, and blood pressure and volume. The anatomical and physiological mechanisms underlying integration of the neuroendocrine and autonomic mechanisms responsible for eliciting integrated autonomic and neuroendocrine actions are the focus of this article. This includes a focus on the hypothalamic paraventricular nucleus, because it includes both neuroendocrine neurons and preganglionic autonomic neurons that regulate sympathetic and parasympathetic outflow. The “wired” and “nonwired” mechanisms within PVN that facilitate communication between these neuronal populations are described. The impact of peripheral hormones, specifically the adrenal and gonadal steroids, on the neuroendocrine and autonomic systems is discussed, and exercise is used as a specific example of a physiological challenge/stress that requires precise integration of neuroendocrine and autonomic responses to maintain cardiovascular, fluid, and energy homeostasis. © 2015 American Physiological Society. Compr Physiol 5:1281‐1323, 2015.

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Figure 1. Figure 1. Schematic representation of medullary and supramedullary nuclei and pathways involved in ANS control. Arrow colors represent the different neurotransmitters: Yellow, excitatory amino‐acids; green, GABA; blue, acetylcholine; red, norepinephrine (NE); light blue, oxytocin (OT); light brown, vasopressin (VP); orange, CRH. ANS, autonomic nervous system including the sympathetic (S) and parasympathetic (P) innervations of heart, blood vessels, and other peripheral organs and tissues; DMV, dorsal motor nucleus of the vagus; IML, intermediolateral cell column of the spinal cord; NA, nucleus ambiguous; NE, noradrenergic ascending pathway; NTS, nucleus of the solitary tract; OT, oxytocinergic descending pathway; PVN, paraventricular nucleus of the hypothalamus; S. gl., sympathetic ganglia; VLM, ventrolateral medulla including the caudal ventrolateral (CVLM) and the rostroventrolateral nuclei (RVLM); VP, vasopressinergic descending pathway. Modified, with permission, from (234).
Figure 2. Figure 2. Topographical organization of functional cell groupings in the rat hypothalamic paraventricular nucleus (PVN). (A) Scheme of the PVN highlighting the different anatomical subdivisions containing neurons that project to the median eminence (gray color, mpd: medial parvocellular subdivision dorsal containing the CRF neurons of the HPA axis; pv: periventricular subnucleus), posterior pituitary (red and green colors, containing primarily oxytocin and VP neurons, respectively; pml: posterior magnocellular latera, pmm, posterior magnocellular medial) or brainstem/spinal cord (blue color, dp: dorsal parvocellular subnucleus, lp: lateral parvocellular subnucleus, mpv: medial parvocellular ventral subnucleus. (B) Rostrocaudal coronal sections of the PVN depicting immunoreactive oxytocin (red), VP (green), and presympathetic retrogradely labeled neurons that innervate the RVLM (blue). Upper, middle, and lower panels correspond to Bregma = −1.3, −1.80, and −2.10, respectively. Scale bar: 100 μm. 3V: third ventricle. (A) Modified from (366) with permission. (C) VP and OT projections from the PVN and SON shown in coronal section of rat brain by immunohistochemical labelling of neurophysin and imaged with darkfield illumination. The antibody used recognizes rat neurophysin which is a component of the prohormones for both VP and OT. The rostrocaudal level of this section is similar to the middle panel of B. (e.g., Bregma ∼−1.8), and thus the darkfield illumination used for this image effectively illustrates the trajectory and density of the HNS axonal projections from the magnocellular VP and OT neurons in PVN as they course laterally and then ventrally to join the axons from SON before passing caudally through the median eminence to the neurohypophysis. Several groups of accessory magnocellular neurons are evident amongst the axons (*). Courtesy of John R. Sladek, Jr., Ph.D.
Figure 3. Figure 3. Integration of the HPA axis and ANS. The HPA axis begins at the level of the hypothalamic PVN where the CRH neurons are located. Release of CRH into portal system, together with VP, increases the secretion of ACTH from the anterior pituitary. Circulating ACTH activates receptors on the adrenal cortex to stimulate the synthesis and release of glucocorticoids (GCs) into the blood. GCs negatively feedback at the levels of the limbic system, hypothalamus, and pituitary to modulate the activity of the HPA axis (dotted blue lines). GCs also contribute to the regulation of blood pressure and plasma renin concentration through increasing angiotensinogen (Aogen) levels [dotted blue line (426)]. The ANS provides the parasympathetic (green) and sympathetic (red) innervation to a number of peripheral sites to modulate blood pressure and heart rate as well as other physiological systems. Parasympathetic activity is associated with decreases in heart rate and blood pressure. Sympathetic neurons (red) stimulate the release of catecholamines from the adrenal medulla and renin secretion from the kidney. Renin catalyzes the rate‐limiting step [angiotensinogen to angiotensin 1 (ANGI)] in ANGII formation. ANGII activates the SFO and OVLT to increase fluid intake and influence the activity of CRH neurons in the PVN. Psychogenic stress is relayed from the limbic system to the CRH neurons via the BNST and hippocampus. The BNST integrates input from other limbic structures including the amygdala (MeA and CeA) PFC, and vSub of the hippocampus. This represents a tightly regulated homeostatic system which, when perturbed, results in a finely tuned and appropriate stress response.
Figure 4. Figure 4. Schematic representation of the regulation of VP and OT release from the neurohypophysis (NH), and their respective roles in maintenance of blood pressure (BP), and volume. The antidiuretic action of VP is important for correcting decreases in blood volume while the natriuretic action of OT [via stimulation of atrial natriuretic hormone release (ANH)] is important for correcting hypervolemia. Although both VP and OT magnocellular neurons are stimulated by increases in osmolality of the extracellular fluid (360) and decreases in blood pressure and volume (281), the hormones are differentially affected by increases in blood volume: hypervolemia causes inhibition of VP and stimulation of OT release from the NH (75). Although information about both increases and decreases in blood volume activate catecholaminergic brainstem afferents, A1 afferents transmit information about a decrease in volume to the magnocellular neurons while information about volume expansion involves a pathway from the locus coeruleus to the BNST and subsequent activation of perinuclear interneurons (75,117). OC: optic chiasma. Reproduced, with permission, from (231).
Figure 5. Figure 5. Innervation of SON by the A1 catecholamine pathway and the impact of coreleased neurotransmitters from this pathway on VP release from explants of the hypothalamo‐neurohypophyseal system (HNS). (A) Histofluorescence demonstration of catecholamine innervation of the SON. Note the intense innervation surrounding individual SON neurons (*). For more detailed descripition and analysis, see (222,334). Image courtesy of John R. Sladek, Jr., Ph.D. (B) Effect of ATP and phenylephrine (PE; to selectively mimic the effect of NE on α1‐adrenergic receptors) on VP release. ATP and PE were added independently or together (ATP/PE) to the perifusion medium at the time indicated by the arrow. Individually, both ATP and PE induce significant, but small and transient increases in VP release from the neurohypophysis. However, when ATP and PE are added simultaneously, the response is larger than the sum of the responses to ATP and PE alone and the increase in VP release is sustained for hours. Adapted, with permission, from (169). (C) ATP also potentiates the response to substance P (sp). However SP alone elicits a sustained increase in VP release. Adapted, with permission, from (170).
Figure 6. Figure 6. Anatomical interrelationships between magnocellular neurosecretory and presympathetic PVN neurons. (A1) Image depicting the topographical segregation between immunoreactive magnocellular VP neurons (green) and retrogradely labeled presympathetic PVN‐RVLM neurons (red). In (A2) and (A3), the squared regions are shown at progressively higher magnification, to better depict the presence of thick and varicose VP dendrites within the presympathetic neuronal compartment. (B1) Image showing retrogradely labeled PVN‐RVLM neurons (blue) and V1a receptor immunoreactivity (green, B2) in the PVN. In B3, the squared area in B1 is shown at an expanded scale to better depict V1a immunoreactive clusters (arrows) located at the surface of the shown dendrite. (C) Single‐cell V1a mRNA expression in identified PVN‐RVLM and eGFP‐VP neurons. A nontemplate negative control is shown in the right lane, and a small piece of a DNA ladder is shown in the left lane. Scale bars: A1 and B1: 20 μm, B3: 2.5 μm. Vertical and horizontal bars in A1 point dorsally and medially, respectively. Modified from (338) with permission.
Figure 7. Figure 7. Dendritic release of VP mediates crosstalk between magnocelluar neurosecretory and presympathetic PVN neurons. (A1) Sample of a hypothalamic slice obtained from an eGFP‐VP rat in which presympathetic PVN neurons were retrogradely labeled following an injection of a fluorescent retrograde tracer in the RVLM. A patched presympathetic PVN‐RVLM neuron (red, asterisk) and neighboring eGFP‐VP neurons (green, 1‐4) are depicted. (A2) Photolysis of caged NMDA onto eGFP‐VP neurons (1,2, orange flashes) evoked delayed bursts of action potentials in the patched presympathetic neuron. Note the delayed response in the PVN‐RVLM neurons compared to B2. (A3) Summary data of mean changes in the number of action potentials, action potential frequency, and membrane potential in presympathetic PVN‐RVLM neurons evoked by photolysis of caged‐NMDA onto eGFP‐VP neurons in the absence or presence of the V1a receptor antagonist. *P < 0.01 and **P < 0.001 versus respective control (ACSF). (B1) Sample pair of intracellularly labeled (Alexa 633, blue, arrows) PVN neurons during simultaneous dual‐patch recordings. Note the identity of the patched neurons as eGFP‐VP (cyan, single arrow) and retrogradely labeled PVN‐RVLM (purple, double arrow). (B2) Electrically evoked bursting activity in the eGFP‐VP neuron resulted in a delayed membrane depolarization and increased firing discharge in the neighboring PVN‐RVLM neuron. (B3) Summary data of mean changes in PVN‐RVLM firing activity following direct stimulation of eGFP‐VP neurons in control ACSF, V1a antagonist or with intracellular BAPTA in the stimulated eGFP‐VP neuron. +P < 0.05 and #P < 0.01 versus V1a antagonist and BAPTA, respectively. Modified from (338) with permission.
Figure 8. Figure 8. A diffusible pool of dendritically released VP tonically modulates presympathetic neuronal activity and contributes to sympathoexcitatory responses during an osmotic challenge. (A1) Bath application of a V1a receptor blocker (1 μmol/L) hyperpolarized and diminished the ongoing firing activity of a presympathetic PVN‐RVLM neuron. At the arrow, DC current injection was applied to bring the membrane potential back to control levels, to show that the V1a antagonist efficiently blocked the neuronal response to a focal application of VP (1 μmol/L, arrowhead). (A2) Summary data showing a significant decrease in PVN‐RVLM firing activity evoked by a V1a receptor antagonist. **P < 0.01. (B1) Representative traces showing changes in renal sympathetic nerve activity (RSNA) following intracarotid infusions of an isosmotic (NaCl 0.3 Osmol/L) or hyperosmotic (NaCl 2.1 Osmol/L) following bilateral microinjections of ACSF or the V1a receptor antagonist onto the PVN. (B2) Mean data showing dose‐dependent increases in RSNA after the intracarotid infusions of NaCl in rats that received an intra‐PVN microinjection of ACSF or the V1a receptor antagonist (*P < 0.0001 vs. respective ACSF). (B3) Increased intranuclear VP content in 30‐min microdialysates before and after an intracarotid infusion of NaCl 2.1 Osmol/L (arrow) (*P < 0.05 vs. basal). Modified from (338) with permission.
Figure 9. Figure 9. Left upper panel: VP release by PVN projections in the nucleus of solitary tract (NTS), rostroventolateral medulla (RVLM) and spinal cord (SC) immediately after an acute bout of exercise in a treadmill in sedentary (S) and trained (T) normotensive rats. *P < 0.05; significant increase in VP after an acute bout of exercise on the treadmill (difference between exercise—resting condition). Left lower panel: Comparison of exercise tachycardia (HR response) to an acute bout of exercise in S(A) and T (B) rats after vehicle (VEH) or VP antagonist (VPant) administration in the NTS. Observe significant decreases of exercise tachycardia following V1 receptors blockade in both groups of rats. *P < 0.05. Modified, with permission, from (94). Right upper panel: OT release by PVN projections in the solitary vagal complex (NTS/DMV), rostroventolateral medulla (RVLM), and spinal cord (SC) immediately after an acute bout of exercise in a treadmill in sedentary (S) and trained (T) normotensive rats. *P < 0.05; significant increase in OT after an acute bout of exercise on the treadmill (difference between exercise—resting condition). Right lower panel: Comparison of exercise tachycardia (HR response) to an acute bout of exercise in S (C) and T rats (D) after vehicle (VEH) or OT antagonist (OTant) administration in the solitary‐vagal complex (NTS/DMV). Observe the significant increase of exercise tachycardia following OT receptors blockade only in trained rats. *P < 0.05. Modified, with permission, from (37).
Figure 10. Figure 10. Left upper panel: Effects of VP (VP), V1 antagonist (VPant), and vehicle (VEH) in the nucleus of the solitary tract (NTS) on the baroreceptor reflex control of heart rate (ΔHR) in rats. Observe the significant upward and rightward displacement of the reflex HR response following VP administration and the absence of reflex bradycardia after V1 receptors blockade. Reproduced, with permission, from (232). Left lower panel: Instantaneous upward and rightward resetting of baroreflex control of heart rate during acute bouts of exercise at different intensities. Modified from (291) with permission. Right upper panel: Displacement of baroreflex function (indicated by the intercept of linear regression equation) induced by VP (VP) administration in the NTS of rats treated intravenously with propranolol (sympathetic blockade), atropine (vagal blockade) or vehicle (VEH). Significances: * versus control; † versus iv blockade. Redrawn, with permission, from data presented in (229). Right lower panel: Excitatory postsynaptic currents (EPSC) evoked by solitary tract stimulation in second order NTS neurons showing two distinct modes of VP (AVP) action to inhibit solitary tract transmission: depressed EPSC amplitude (V1 receptors located on solitary tract terminals—A, inset) or intermittent EPSC failures (red current traces, when V1 receptors are distant from the terminal release site—B, inset). Calibration: 10 ms, 100 pA. Reproduced from (19) with permission.
Figure 11. Figure 11. Left panel: Effects of OT (OT), OT antagonist (OTant), and vehicle (VEH) in the solitary‐vagal complex (NTS/DMV) on the baroreceptor reflex control of heart rate (HR) in rats. Baroreflex induced by loading and unloading of the baroreceptors with IV phenylephrine/sodium nitroprusside. * denotes a significant difference, P < 0.05. Reproduced, with permission, from (152). Right upper panel: Changes in the sensitivity (slope) of baroreflex control of heart rate induced by OT (OT) administration in the solitary‐vagal complex in rats treated intravenously with atenolol (sympathetic blockade), atropine (vagal blockade), or vehicle (VEH). Significances: * versus control; † versus iv blockade. Redrawn, with permission, from data presented in (152). Right lower panel: Miniature excitatory postsynaptic currents (mEPSC) recorded in second‐order NTS neurons in basal condition (control) and after topic administration of OT (OT) in the absence or presence of OT antagonist (Antag): A—representative current traces; B—frequency data plotted over time; and C—normalized group data under each condition. Reproduced from (275) with permission.
Figure 12. Figure 12. Upper panel: Comparison of baroreceptor reflex control of heart rate in intact (SHAM) sedentary (S) and trained (T) rats. Modified, with permission, from (52). Lower panel: Photomicrographs showing OT immunofluorescence (OTif) in the paraventricular nucleus of the hypothalamus in representative intact (SHAM) sedentary (S) and trained (T) rats. Note the augmented OTif after training (increased OTif density in cell bodies and projections). DC, dorsal cap nucleus; Mg, magnocellular nucleus; VM, ventromedial nucleus; 3V, third ventricle
Figure 13. Figure 13. Decrease in ERβ expression in SON with dehydration. (A and B) In situ hybridization for ERβ mRNA. (C and D) Immunohistochemistry for ERβ. (E and F) Double immunohistochemistry for OT (brown reaction product) and ERβ (dark blue) in SON from control and water deprived rats. ERβ is prominently expressed in the VP neurons in rat SON. Seventy‐two hours of water deprivation depletes ERβ mRNA (B) as well as immunoreactivity (D). Reprinted, with permission, from (333).
Figure 14. Figure 14. Hormonal changes across a normal menstrual cycle. LH (luteinizing hormone), FSH (follicle stimulating hormone). Note that actual levels of estradiol, progesterone, LH, and FSH are approximate because these vary across individuals (347).
Figure 15. Figure 15. Estradiol and progesterone changes in response to GnRH agonist (leuprolide, top) and GnRH antagonist (ganirelix, bottom). Note that actual levels of estradiol, progesterone, LH, and FSH are approximate because these vary across individuals (349).
Figure 16. Figure 16. The relationship of MSNA to total peripheral resistance in men and women. (TPR; top panels) and cardiac output (CO; bottom panels) in young men (left) and young women (right) MSNA (bursts per 100 heart beats) is positively related to TPR but inversely related to cardiac output in young men. Conversely, there is no relationship among MSNA, TPR and cardiac output in young women. Data taken, with permission, from Charkoudian et al. (56,57,58) and Hart et al. (134,135). Figure used with permission from (136).
Figure 17. Figure 17. ERα expression in neurons in the osmosensitive components of the lamina terminalis. A. Diagram showing location of the circumventricular organs in the anterior hypothalamus that monitor extracellular fluid osmolality, for example, subfornical organ (SFO) and organum vasculosum of the lamina terminalis (OVLT). (B‐E) Sections through SFO (B and C) and OVLT (D and E) from 48 h water deprived rats were double stained for ERα (green) and Fos (red). The rectangles in B and D indicate regions shown at higher magnification in C and E, respectively. Fos staining is indicative of neurons activated by the dehydration protocol, and numerous ERα positive neurons show Fos activation (yellow/orange, some indicted by white arrowheads in C and E). Scale bars, 50 mm. Reproduced with permission from (333).
Figure 18. Figure 18. Comparison of osmotic regulation of VP secretion and thirst in men and in women at different stages of the menstrual cycle. (A and B) Osmotic regulation of pVP (P[AVP]) and thirst during hypertonic saline infusion. (A) Women (follicular phase): f(x) = 0.14*x + −273, R2 = 0.97; women (luteal phase): f(x) = 0.09*x + −263, R2 = 0.89; Men: f(x) = 0.24*x + −270, R2 = 0.99. Adapted, with permission, from Stachenfeld et al. (347). (B) Thirst during hypertonic saline infusion. Adapted from Calzone et al. (45). (C and D) Osmotic regulation of P[AVP] and thirst in women during the follicular and luteal phases of the menstrual cycle during exercise‐induced dehydration. Follicular phase: f(x) = 0.47*x + −283, Luteal phase: f(x) = 0.51*x + −278. Adapted, with permission, from Stachenfeld et al. (346346). Data are expressed as mean ± SEM.


Figure 1. Schematic representation of medullary and supramedullary nuclei and pathways involved in ANS control. Arrow colors represent the different neurotransmitters: Yellow, excitatory amino‐acids; green, GABA; blue, acetylcholine; red, norepinephrine (NE); light blue, oxytocin (OT); light brown, vasopressin (VP); orange, CRH. ANS, autonomic nervous system including the sympathetic (S) and parasympathetic (P) innervations of heart, blood vessels, and other peripheral organs and tissues; DMV, dorsal motor nucleus of the vagus; IML, intermediolateral cell column of the spinal cord; NA, nucleus ambiguous; NE, noradrenergic ascending pathway; NTS, nucleus of the solitary tract; OT, oxytocinergic descending pathway; PVN, paraventricular nucleus of the hypothalamus; S. gl., sympathetic ganglia; VLM, ventrolateral medulla including the caudal ventrolateral (CVLM) and the rostroventrolateral nuclei (RVLM); VP, vasopressinergic descending pathway. Modified, with permission, from (234).


Figure 2. Topographical organization of functional cell groupings in the rat hypothalamic paraventricular nucleus (PVN). (A) Scheme of the PVN highlighting the different anatomical subdivisions containing neurons that project to the median eminence (gray color, mpd: medial parvocellular subdivision dorsal containing the CRF neurons of the HPA axis; pv: periventricular subnucleus), posterior pituitary (red and green colors, containing primarily oxytocin and VP neurons, respectively; pml: posterior magnocellular latera, pmm, posterior magnocellular medial) or brainstem/spinal cord (blue color, dp: dorsal parvocellular subnucleus, lp: lateral parvocellular subnucleus, mpv: medial parvocellular ventral subnucleus. (B) Rostrocaudal coronal sections of the PVN depicting immunoreactive oxytocin (red), VP (green), and presympathetic retrogradely labeled neurons that innervate the RVLM (blue). Upper, middle, and lower panels correspond to Bregma = −1.3, −1.80, and −2.10, respectively. Scale bar: 100 μm. 3V: third ventricle. (A) Modified from (366) with permission. (C) VP and OT projections from the PVN and SON shown in coronal section of rat brain by immunohistochemical labelling of neurophysin and imaged with darkfield illumination. The antibody used recognizes rat neurophysin which is a component of the prohormones for both VP and OT. The rostrocaudal level of this section is similar to the middle panel of B. (e.g., Bregma ∼−1.8), and thus the darkfield illumination used for this image effectively illustrates the trajectory and density of the HNS axonal projections from the magnocellular VP and OT neurons in PVN as they course laterally and then ventrally to join the axons from SON before passing caudally through the median eminence to the neurohypophysis. Several groups of accessory magnocellular neurons are evident amongst the axons (*). Courtesy of John R. Sladek, Jr., Ph.D.


Figure 3. Integration of the HPA axis and ANS. The HPA axis begins at the level of the hypothalamic PVN where the CRH neurons are located. Release of CRH into portal system, together with VP, increases the secretion of ACTH from the anterior pituitary. Circulating ACTH activates receptors on the adrenal cortex to stimulate the synthesis and release of glucocorticoids (GCs) into the blood. GCs negatively feedback at the levels of the limbic system, hypothalamus, and pituitary to modulate the activity of the HPA axis (dotted blue lines). GCs also contribute to the regulation of blood pressure and plasma renin concentration through increasing angiotensinogen (Aogen) levels [dotted blue line (426)]. The ANS provides the parasympathetic (green) and sympathetic (red) innervation to a number of peripheral sites to modulate blood pressure and heart rate as well as other physiological systems. Parasympathetic activity is associated with decreases in heart rate and blood pressure. Sympathetic neurons (red) stimulate the release of catecholamines from the adrenal medulla and renin secretion from the kidney. Renin catalyzes the rate‐limiting step [angiotensinogen to angiotensin 1 (ANGI)] in ANGII formation. ANGII activates the SFO and OVLT to increase fluid intake and influence the activity of CRH neurons in the PVN. Psychogenic stress is relayed from the limbic system to the CRH neurons via the BNST and hippocampus. The BNST integrates input from other limbic structures including the amygdala (MeA and CeA) PFC, and vSub of the hippocampus. This represents a tightly regulated homeostatic system which, when perturbed, results in a finely tuned and appropriate stress response.


Figure 4. Schematic representation of the regulation of VP and OT release from the neurohypophysis (NH), and their respective roles in maintenance of blood pressure (BP), and volume. The antidiuretic action of VP is important for correcting decreases in blood volume while the natriuretic action of OT [via stimulation of atrial natriuretic hormone release (ANH)] is important for correcting hypervolemia. Although both VP and OT magnocellular neurons are stimulated by increases in osmolality of the extracellular fluid (360) and decreases in blood pressure and volume (281), the hormones are differentially affected by increases in blood volume: hypervolemia causes inhibition of VP and stimulation of OT release from the NH (75). Although information about both increases and decreases in blood volume activate catecholaminergic brainstem afferents, A1 afferents transmit information about a decrease in volume to the magnocellular neurons while information about volume expansion involves a pathway from the locus coeruleus to the BNST and subsequent activation of perinuclear interneurons (75,117). OC: optic chiasma. Reproduced, with permission, from (231).


Figure 5. Innervation of SON by the A1 catecholamine pathway and the impact of coreleased neurotransmitters from this pathway on VP release from explants of the hypothalamo‐neurohypophyseal system (HNS). (A) Histofluorescence demonstration of catecholamine innervation of the SON. Note the intense innervation surrounding individual SON neurons (*). For more detailed descripition and analysis, see (222,334). Image courtesy of John R. Sladek, Jr., Ph.D. (B) Effect of ATP and phenylephrine (PE; to selectively mimic the effect of NE on α1‐adrenergic receptors) on VP release. ATP and PE were added independently or together (ATP/PE) to the perifusion medium at the time indicated by the arrow. Individually, both ATP and PE induce significant, but small and transient increases in VP release from the neurohypophysis. However, when ATP and PE are added simultaneously, the response is larger than the sum of the responses to ATP and PE alone and the increase in VP release is sustained for hours. Adapted, with permission, from (169). (C) ATP also potentiates the response to substance P (sp). However SP alone elicits a sustained increase in VP release. Adapted, with permission, from (170).


Figure 6. Anatomical interrelationships between magnocellular neurosecretory and presympathetic PVN neurons. (A1) Image depicting the topographical segregation between immunoreactive magnocellular VP neurons (green) and retrogradely labeled presympathetic PVN‐RVLM neurons (red). In (A2) and (A3), the squared regions are shown at progressively higher magnification, to better depict the presence of thick and varicose VP dendrites within the presympathetic neuronal compartment. (B1) Image showing retrogradely labeled PVN‐RVLM neurons (blue) and V1a receptor immunoreactivity (green, B2) in the PVN. In B3, the squared area in B1 is shown at an expanded scale to better depict V1a immunoreactive clusters (arrows) located at the surface of the shown dendrite. (C) Single‐cell V1a mRNA expression in identified PVN‐RVLM and eGFP‐VP neurons. A nontemplate negative control is shown in the right lane, and a small piece of a DNA ladder is shown in the left lane. Scale bars: A1 and B1: 20 μm, B3: 2.5 μm. Vertical and horizontal bars in A1 point dorsally and medially, respectively. Modified from (338) with permission.


Figure 7. Dendritic release of VP mediates crosstalk between magnocelluar neurosecretory and presympathetic PVN neurons. (A1) Sample of a hypothalamic slice obtained from an eGFP‐VP rat in which presympathetic PVN neurons were retrogradely labeled following an injection of a fluorescent retrograde tracer in the RVLM. A patched presympathetic PVN‐RVLM neuron (red, asterisk) and neighboring eGFP‐VP neurons (green, 1‐4) are depicted. (A2) Photolysis of caged NMDA onto eGFP‐VP neurons (1,2, orange flashes) evoked delayed bursts of action potentials in the patched presympathetic neuron. Note the delayed response in the PVN‐RVLM neurons compared to B2. (A3) Summary data of mean changes in the number of action potentials, action potential frequency, and membrane potential in presympathetic PVN‐RVLM neurons evoked by photolysis of caged‐NMDA onto eGFP‐VP neurons in the absence or presence of the V1a receptor antagonist. *P < 0.01 and **P < 0.001 versus respective control (ACSF). (B1) Sample pair of intracellularly labeled (Alexa 633, blue, arrows) PVN neurons during simultaneous dual‐patch recordings. Note the identity of the patched neurons as eGFP‐VP (cyan, single arrow) and retrogradely labeled PVN‐RVLM (purple, double arrow). (B2) Electrically evoked bursting activity in the eGFP‐VP neuron resulted in a delayed membrane depolarization and increased firing discharge in the neighboring PVN‐RVLM neuron. (B3) Summary data of mean changes in PVN‐RVLM firing activity following direct stimulation of eGFP‐VP neurons in control ACSF, V1a antagonist or with intracellular BAPTA in the stimulated eGFP‐VP neuron. +P < 0.05 and #P < 0.01 versus V1a antagonist and BAPTA, respectively. Modified from (338) with permission.


Figure 8. A diffusible pool of dendritically released VP tonically modulates presympathetic neuronal activity and contributes to sympathoexcitatory responses during an osmotic challenge. (A1) Bath application of a V1a receptor blocker (1 μmol/L) hyperpolarized and diminished the ongoing firing activity of a presympathetic PVN‐RVLM neuron. At the arrow, DC current injection was applied to bring the membrane potential back to control levels, to show that the V1a antagonist efficiently blocked the neuronal response to a focal application of VP (1 μmol/L, arrowhead). (A2) Summary data showing a significant decrease in PVN‐RVLM firing activity evoked by a V1a receptor antagonist. **P < 0.01. (B1) Representative traces showing changes in renal sympathetic nerve activity (RSNA) following intracarotid infusions of an isosmotic (NaCl 0.3 Osmol/L) or hyperosmotic (NaCl 2.1 Osmol/L) following bilateral microinjections of ACSF or the V1a receptor antagonist onto the PVN. (B2) Mean data showing dose‐dependent increases in RSNA after the intracarotid infusions of NaCl in rats that received an intra‐PVN microinjection of ACSF or the V1a receptor antagonist (*P < 0.0001 vs. respective ACSF). (B3) Increased intranuclear VP content in 30‐min microdialysates before and after an intracarotid infusion of NaCl 2.1 Osmol/L (arrow) (*P < 0.05 vs. basal). Modified from (338) with permission.


Figure 9. Left upper panel: VP release by PVN projections in the nucleus of solitary tract (NTS), rostroventolateral medulla (RVLM) and spinal cord (SC) immediately after an acute bout of exercise in a treadmill in sedentary (S) and trained (T) normotensive rats. *P < 0.05; significant increase in VP after an acute bout of exercise on the treadmill (difference between exercise—resting condition). Left lower panel: Comparison of exercise tachycardia (HR response) to an acute bout of exercise in S(A) and T (B) rats after vehicle (VEH) or VP antagonist (VPant) administration in the NTS. Observe significant decreases of exercise tachycardia following V1 receptors blockade in both groups of rats. *P < 0.05. Modified, with permission, from (94). Right upper panel: OT release by PVN projections in the solitary vagal complex (NTS/DMV), rostroventolateral medulla (RVLM), and spinal cord (SC) immediately after an acute bout of exercise in a treadmill in sedentary (S) and trained (T) normotensive rats. *P < 0.05; significant increase in OT after an acute bout of exercise on the treadmill (difference between exercise—resting condition). Right lower panel: Comparison of exercise tachycardia (HR response) to an acute bout of exercise in S (C) and T rats (D) after vehicle (VEH) or OT antagonist (OTant) administration in the solitary‐vagal complex (NTS/DMV). Observe the significant increase of exercise tachycardia following OT receptors blockade only in trained rats. *P < 0.05. Modified, with permission, from (37).


Figure 10. Left upper panel: Effects of VP (VP), V1 antagonist (VPant), and vehicle (VEH) in the nucleus of the solitary tract (NTS) on the baroreceptor reflex control of heart rate (ΔHR) in rats. Observe the significant upward and rightward displacement of the reflex HR response following VP administration and the absence of reflex bradycardia after V1 receptors blockade. Reproduced, with permission, from (232). Left lower panel: Instantaneous upward and rightward resetting of baroreflex control of heart rate during acute bouts of exercise at different intensities. Modified from (291) with permission. Right upper panel: Displacement of baroreflex function (indicated by the intercept of linear regression equation) induced by VP (VP) administration in the NTS of rats treated intravenously with propranolol (sympathetic blockade), atropine (vagal blockade) or vehicle (VEH). Significances: * versus control; † versus iv blockade. Redrawn, with permission, from data presented in (229). Right lower panel: Excitatory postsynaptic currents (EPSC) evoked by solitary tract stimulation in second order NTS neurons showing two distinct modes of VP (AVP) action to inhibit solitary tract transmission: depressed EPSC amplitude (V1 receptors located on solitary tract terminals—A, inset) or intermittent EPSC failures (red current traces, when V1 receptors are distant from the terminal release site—B, inset). Calibration: 10 ms, 100 pA. Reproduced from (19) with permission.


Figure 11. Left panel: Effects of OT (OT), OT antagonist (OTant), and vehicle (VEH) in the solitary‐vagal complex (NTS/DMV) on the baroreceptor reflex control of heart rate (HR) in rats. Baroreflex induced by loading and unloading of the baroreceptors with IV phenylephrine/sodium nitroprusside. * denotes a significant difference, P < 0.05. Reproduced, with permission, from (152). Right upper panel: Changes in the sensitivity (slope) of baroreflex control of heart rate induced by OT (OT) administration in the solitary‐vagal complex in rats treated intravenously with atenolol (sympathetic blockade), atropine (vagal blockade), or vehicle (VEH). Significances: * versus control; † versus iv blockade. Redrawn, with permission, from data presented in (152). Right lower panel: Miniature excitatory postsynaptic currents (mEPSC) recorded in second‐order NTS neurons in basal condition (control) and after topic administration of OT (OT) in the absence or presence of OT antagonist (Antag): A—representative current traces; B—frequency data plotted over time; and C—normalized group data under each condition. Reproduced from (275) with permission.


Figure 12. Upper panel: Comparison of baroreceptor reflex control of heart rate in intact (SHAM) sedentary (S) and trained (T) rats. Modified, with permission, from (52). Lower panel: Photomicrographs showing OT immunofluorescence (OTif) in the paraventricular nucleus of the hypothalamus in representative intact (SHAM) sedentary (S) and trained (T) rats. Note the augmented OTif after training (increased OTif density in cell bodies and projections). DC, dorsal cap nucleus; Mg, magnocellular nucleus; VM, ventromedial nucleus; 3V, third ventricle


Figure 13. Decrease in ERβ expression in SON with dehydration. (A and B) In situ hybridization for ERβ mRNA. (C and D) Immunohistochemistry for ERβ. (E and F) Double immunohistochemistry for OT (brown reaction product) and ERβ (dark blue) in SON from control and water deprived rats. ERβ is prominently expressed in the VP neurons in rat SON. Seventy‐two hours of water deprivation depletes ERβ mRNA (B) as well as immunoreactivity (D). Reprinted, with permission, from (333).


Figure 14. Hormonal changes across a normal menstrual cycle. LH (luteinizing hormone), FSH (follicle stimulating hormone). Note that actual levels of estradiol, progesterone, LH, and FSH are approximate because these vary across individuals (347).


Figure 15. Estradiol and progesterone changes in response to GnRH agonist (leuprolide, top) and GnRH antagonist (ganirelix, bottom). Note that actual levels of estradiol, progesterone, LH, and FSH are approximate because these vary across individuals (349).


Figure 16. The relationship of MSNA to total peripheral resistance in men and women. (TPR; top panels) and cardiac output (CO; bottom panels) in young men (left) and young women (right) MSNA (bursts per 100 heart beats) is positively related to TPR but inversely related to cardiac output in young men. Conversely, there is no relationship among MSNA, TPR and cardiac output in young women. Data taken, with permission, from Charkoudian et al. (56,57,58) and Hart et al. (134,135). Figure used with permission from (136).


Figure 17. ERα expression in neurons in the osmosensitive components of the lamina terminalis. A. Diagram showing location of the circumventricular organs in the anterior hypothalamus that monitor extracellular fluid osmolality, for example, subfornical organ (SFO) and organum vasculosum of the lamina terminalis (OVLT). (B‐E) Sections through SFO (B and C) and OVLT (D and E) from 48 h water deprived rats were double stained for ERα (green) and Fos (red). The rectangles in B and D indicate regions shown at higher magnification in C and E, respectively. Fos staining is indicative of neurons activated by the dehydration protocol, and numerous ERα positive neurons show Fos activation (yellow/orange, some indicted by white arrowheads in C and E). Scale bars, 50 mm. Reproduced with permission from (333).


Figure 18. Comparison of osmotic regulation of VP secretion and thirst in men and in women at different stages of the menstrual cycle. (A and B) Osmotic regulation of pVP (P[AVP]) and thirst during hypertonic saline infusion. (A) Women (follicular phase): f(x) = 0.14*x + −273, R2 = 0.97; women (luteal phase): f(x) = 0.09*x + −263, R2 = 0.89; Men: f(x) = 0.24*x + −270, R2 = 0.99. Adapted, with permission, from Stachenfeld et al. (347). (B) Thirst during hypertonic saline infusion. Adapted from Calzone et al. (45). (C and D) Osmotic regulation of P[AVP] and thirst in women during the follicular and luteal phases of the menstrual cycle during exercise‐induced dehydration. Follicular phase: f(x) = 0.47*x + −283, Luteal phase: f(x) = 0.51*x + −278. Adapted, with permission, from Stachenfeld et al. (346346). Data are expressed as mean ± SEM.
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Celia D. Sladek, Lisete C. Michelini, Nina S. Stachenfeld, Javier E. Stern, Janice H. Urban. Endocrine‐Autonomic Linkages. Compr Physiol 2015, 5: 1281-1323. doi: 10.1002/cphy.c140028