Sympathetic network drive during water deprivation does not increase respiratory or cardiac rhythmic sympathetic nerve activity

Holbein, Walter W.; Toney, Glenn M.

doi:10.1152/japplphysiol.00078.2013

Cited by 10 publications

(22 citation statements)

References 46 publications

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“…As recently reported (Holbein & Toney, ), for similar values of

{ET}_{{CO}_{2}}

across groups (EH: 5.6 ± 0.2%; DH: 5.5 ± 0.1%), neural inspiratory time (EH: 0.50 ± 0.05 s; DH: 0.51 ± 0.03 s), neural expiratory time (EH: 1.16 ± 0.08 s; DH: 1.05 ± 0.05 s), PNA burst amplitude (EH: 11.9 ± 2.0 μV; DH: 10.8 ± 2.0 μV) and PNA burst AUC (EH: 3.2 ± 0.5 μV.s; DH, 3.6 ± 0.7 μV.s) were all similar in EH and DH rats ( n = 6 per group), indicating that dehydration had no effect on the strength of central respiratory drive. Note that ventilation parameters (depth and frequency) were similar in EH and DH rats and were not affected by PVN inhibition in either group.…”

Section: Resultssupporting

confidence: 85%

“…As previously reported (Stocker et al . , ; Holbein & Toney, ), EH and DH rats had similar baseline values of MAP and HR whereas haematocrit, plasma protein concentration and plasma osmolality were each significantly elevated in the DH group ( P < 0.01). These haematology values indicate that DH rats were both hyperosmotic and hypovolaemic.…”

Section: Resultsmentioning

confidence: 85%

“…However, we recently reported that this is not the case. Instead, dehydration increased a tonic component of splanchnic SNA without changing respiratory or cardiac rhythmic bursting (Holbein & Toney, ). Given this unexpected finding, the present study sought to establish the role of PVN neuronal activity in the patterning of SNA during dehydration by testing the hypothesis that acute inhibition of PVN neuronal activity in dehydrated rats will reduce AP by selectively reducing a tonic component of SNA.…”

Section: Introductionmentioning

confidence: 99%

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Blood pressure is maintained during dehydration by hypothalamic paraventricular nucleus‐driven tonic sympathetic nerve activity

Holbein

Bardgett

Toney

2014

The Journal of Physiology

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Key pointsr At normal resting mean arterial pressure (MAP), sympathetic nerve activity (SNA) mostly consists of respiratory and cardiac rhythmic bursts of action potentials.r In animal models of sympathetic hyperactivity, elevated SNA and MAP become reliant on activity of neurones in the hypothalamic paraventricular nucleus (PVN).r Dehydrated (DH) rats (48 h water deprived) were used as a model of sympathetic hyperactivity.As expected, acute PVN inhibition reduced MAP and integrated splanchnic SNA (sSNA) in DH rats, but had no effect in euhydrated controls. Unexpectedly, the fall of sSNA in DH rats was due to a reduction of irregular, tonic activity as neither respiratory nor cardiac rhythmic bursting was significantly affected.r We conclude that MAP is largely maintained during dehydration by PVN-driven tonic SNA and speculate that a normally quiescent tonic component of SNA might also be recruited in chronic diseases (hypertension, heart failure, obesity) where PVN activation drives sympathetic hyperactivity.Abstract Resting sympathetic nerve activity (SNA) consists primarily of respiratory and cardiac rhythmic bursts of action potentials. During homeostatic challenges such as dehydration, the hypothalamic paraventricular nucleus (PVN) is activated and drives SNA in support of arterial pressure (AP). Given that PVN neurones project to brainstem cardio-respiratory regions that generate bursting patterns of SNA, we sought to determine the contribution of PVN to support of rhythmic bursting of SNA during dehydration and to elucidate which bursts dominantly contribute to maintenance of AP. Euhydrated (EH) and dehydrated (DH) (48 h water deprived) rats were anaesthetized, bilaterally vagotomized and underwent acute PVN inhibition by bilateral injection of the GABA-A receptor agonist muscimol (0.1 nmol in 50 nl). Consistent with previous studies, muscimol had no effect in EH rats (n = 6), but reduced mean AP (MAP; P < 0.001) and integrated splanchnic SNA (sSNA; P < 0.001) in DH rats (n = 6). Arterial pulse pressure was unaffected in both groups. Muscimol reduced burst frequency of phrenic nerve activity (P < 0.05) equally in both groups without affecting the burst amplitude-duration integral (i.e. area under the curve). PVN inhibition did not affect the amplitude of the inspiratory peak, expiratory trough or expiratory peak of sSNA in either group, but reduced cardiac rhythmic sSNA in DH rats only (P < 0.001). The latter was largely reversed by inflating an aortic cuff to restore MAP (n = 5), suggesting that the muscimol-induced reduction of cardiac rhythmic sSNA in DH rats was an indirect effect of reducing MAP and thus arterial baroreceptor input. We conclude that MAP is largely maintained in anaesthetized DH rats by a PVN-driven component of sSNA that is neither respiratory nor cardiac rhythmic.

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“…As recently reported (Holbein & Toney, ), for similar values of

{ET}_{{CO}_{2}}

Section: Resultssupporting

confidence: 85%

Section: Resultsmentioning

confidence: 85%

Section: Introductionmentioning

confidence: 99%

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Blood pressure is maintained during dehydration by hypothalamic paraventricular nucleus‐driven tonic sympathetic nerve activity

Holbein

Bardgett

Toney

2014

The Journal of Physiology

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“…Catheters (PE-50 tubing) were implanted in a femoral artery and vein for recording ABP and administration of drugs, respectively. Because the role of PVN cytokines on various regional sympathetic outflows in Ang II-salt hypertension has not been previously investigated, rats in the present study rats were prepared for recording of renal (RSNA), splanchnic (SSNA), or lumbar (LSNA) SNA as previously described by our laboratory 23–25 . Animals were artificially ventilated with oxygen-enriched room air, paralyzed with gallamine triethiodide (20 mg/mL, 0.25 mL/h, IV) and end tidal CO 2 was monitored and maintained between 4–5%.…”

Section: Methodsmentioning

confidence: 99%

Ang II–Salt Hypertension Depends on Neuronal Activity in the Hypothalamic Paraventricular Nucleus but Not on Local Actions of Tumor Necrosis Factor-α

et al. 2014

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Development of angiotensin II (Ang II)-dependent hypertension involves microglial activation and proinflammatory cytokine actions in the hypothalamic paraventricular nucleus (PVN). Cytokines activate receptor signaling pathways that can both acutely grade neuronal discharge and trigger long-term adaptive changes that modulate neuronal excitability through gene transcription. Here, we investigated contributions of PVN cytokines to maintenance of hypertension induced by infusion of Ang II (150 ng/kg/min, SC) for 14 days in rats consuming a 2% NaCl diet. Results indicate that bilateral PVN inhibition with the GABA-A receptor agonist muscimol (100 pmol/50 nL) caused significantly greater reductions of renal and splanchnic sympathetic nerve activity (SNA) and mean arterial pressure (MAP) in hypertensive than normotensive rats (P<0.01). Thus ongoing PVN neuronal activity appears required for support of hypertension. Next, the role of the prototypical cytokine tumor necrosis factor alpha (TNF-α) was investigated. Whereas PVN injection of TNF-α (0.3 pmol/50 nL) acutely increased lumbar and splanchnic SNA and MAP, interfering with endogenous TNF-α by injection of etanercept (10 µg/50 nL) was without effect in hypertensive and normotensive rats. We next determined that although microglial activation in PVN was increased in hypertensive rats, bilateral injections of minocycline (0.5 µg/50 nL), an inhibitor of microglial activation, failed to reduce lumbar or splanchnic SNA or MAP in hypertensive or normotensive rats. Collectively, these findings indicate that established Ang II-salt hypertension is supported by PVN neuronal activity, but short term maintenance of SNA and ABP does not depend on ongoing local actions of TNF-α.

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“…Catheters (PE-50 tubing) were implanted in a femoral artery and vein to record ABP and administer drugs, respectively. Lumbar and splanchnic SNA were recorded as described previously (1,2,13,29). Animals were artificially ventilated with oxygen-enriched room air and end-tidal CO 2 was monitored and maintained between 4.5 and 5%.…”

Section: In Vivo Studies In Anesthetized Ratsmentioning

confidence: 99%

Activation of corticotropin-releasing factor receptors in the rostral ventrolateral medulla is required for glucose-induced sympathoexcitation

Bardgett¹,

Sharpe

Toney

2014

American Journal of Physiology-Endocrinology and Metabolism

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Energy expenditure is determined by metabolic rate and diet-induced thermogenesis. Normally, energy expenditure increases due to neural mechanisms that sense plasma levels of ingested nutrients/hormones and reflexively increase sympathetic nerve activity (SNA). Here, we investigated neural mechanisms of glucose-driven sympathetic activation by determining contributions of neuronal activity in the hypothalamic paraventricular nucleus (PVN) and activation of corticotropin-releasing factor (CRF) receptors in the rostral ventrolateral medulla (RVLM). Glucose was infused intravenously (150 mg/kg, 10 min) in male rats to raise plasma glucose concentration to a physiological postprandial level. In conscious rats, glucose infusion activated CRF-containing PVN neurons and TH-containing RVLM neurons, as indexed by c-Fos immunofluorescence. In ␣-chloralose/urethane-anesthetized rats, glucose infusion increased lumbar and splanchnic SNA, which was nearly prevented by prior RVLM injection of the CRF receptor antagonist astressin (10 pmol/50 nl). This cannot be attributed to a nonspecific effect, as sciatic afferent stimulation increased SNA and ABP equivalently in astressin-and aCSF-injected rats. Glucose-stimulated sympathoexcitation was largely reversed during inhibition of PVN neuronal activity with the GABA-A receptor agonist muscimol (100 pmol/50 nl). The effects of astressin to prevent glucose-stimulated sympathetic activation appear to be specific to interruption of PVN drive to RVLM because RVLM injection of astressin prior to glucose infusion effectively prevented SNA from rising and prevented any fall of SNA in response to acute PVN inhibition with muscimol. These findings suggest that activation of SNA, and thus energy expenditure, by glucose is initiated by activation of CRF receptors in RVLM by descending inputs from PVN. corticotropin releasing factor; sympathetic nerve activity; rostral ventrolateral medulla DECREASING THE RISK of obesity-related metabolic (e.g., type 2 diabetes) and cardiovascular diseases (hypertension, atherosclerosis, and stroke) is often achieved by weight loss. Normal body weight is maintained by a balance between food intake and energy expenditure, and even small perturbations in this balance can produce large changes in body composition over time. Therefore, it is imperative to understand the neural circuits and synaptic mechanisms that control energy expenditure. Daily energy expenditure is determined by three major components: resting metabolic rate, exercise-induced increases in metabolic rate, and diet-induced thermogenesis (37). Among sedentary individuals, resting metabolic rate is the major determinant of daily energy expenditure and is maintained by a combination of sympathetic nerve activity (SNA), cortisol levels, and thyroid hormones (41, 42). Many features of the neural circuitry that drive energy expenditure, especially through activation of SNA, remain incompletely understood. Food intake stimulates energy expenditure through neural mechanisms that sense the elevation of ...

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Sympathetic network drive during water deprivation does not increase respiratory or cardiac rhythmic sympathetic nerve activity

Cited by 10 publications

References 46 publications

Blood pressure is maintained during dehydration by hypothalamic paraventricular nucleus‐driven tonic sympathetic nerve activity

Blood pressure is maintained during dehydration by hypothalamic paraventricular nucleus‐driven tonic sympathetic nerve activity

Ang II–Salt Hypertension Depends on Neuronal Activity in the Hypothalamic Paraventricular Nucleus but Not on Local Actions of Tumor Necrosis Factor-α

Activation of corticotropin-releasing factor receptors in the rostral ventrolateral medulla is required for glucose-induced sympathoexcitation

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