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Sympathoneural and Adrenomedullary Responses to Mental Stress

Jason R. Carter, David S. Goldstein

10.1002/cphy.c140030

Source: Volume 5, Issue 1, January 2015

Published online: December 2014

Full Article on Wiley Online Library



Abstract

This concept‐based review provides historical perspectives and updates about sympathetic noradrenergic and sympathetic adrenergic responses to mental stress. The topic of this review has incited perennial debate, because of disagreements over definitions, controversial inferences, and limited availability of relevant measurement tools. The discussion begins appropriately with Cannon's “homeostasis” and his pioneering work in the area. This is followed by mental stress as a scientific idea and the relatively new notions of allostasis and allostatic load. Experimental models of mental stress in rodents and humans are discussed, with particular attention to ethical constraints in humans. Sections follow on sympathoneural responses to mental stress, reactivity of catecholamine systems, clinical pathophysiologic states, and the cardiovascular reactivity hypothesis. Future advancement of the field will require integrative approaches and coordinated efforts between physiologists and psychologists on this interdisciplinary topic. Published 2015. Compr Physiol 5:119‐146, 2015.

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Figure 1. Figure 1. Original recordings of muscle sympathetic nerve activity (MSNA) and beat‐to‐beat arterial blood pressure during acute, laboratory‐based mental stress. Taken with permission from Wallin et al. (279).
Figure 2. Figure 2. Muscle sympathetic nerve activity (MSNA) responsiveness to mental stress was not correlated to arterial blood pressure responsiveness; DAP, diastolic arterial pressure. Taken with permission from Carter & Ray (39).
Figure 3. Figure 3. Mental stress increases forearm vascular conductance (FVC) without any change in forearm muscle sympathetic nerve activity (MSNA); VOP, venous occlusion plethysmography; DOPPLER, Doppler ultrasound technique; B, baseline; R, recovery. Modified with permission from Carter et al. (37).
Figure 4. Figure 4. Muscle sympathetic nerve activity correlates strongly with femoral venous (FV) plasma norepinephrine (NE) concentrations and spillover at rest, but not during mental stress elicited via Stroop's color word conflict test (CWT). Taken with permission from Hjemdahl et al. (133).
Figure 5. Figure 5. Skin sympathetic nerve activity (SSNA) responsiveness to mental stress was divergent in the tibial (T) and peroneal (P) nerves of hyperhidrosis patients. Taken with permission from Iwase et al. (137).
Figure 6. Figure 6. Skin sympathetic nerve activity (SSNA) responses to emotionally charged images from the International Affective Picture System (IAPS). Taken with permission from Brown et al. (24).
Figure 7. Figure 7. Panic disorder (PD) patient peripheral sympathetic neurons fire more often in a “multiple spike” pattern when compared to health controls. Taken with permission from Lambert et al. (172).
Figure 8. Figure 8. Hemodynamic and catecholamine responses to mental challenge (playing a video game) in healthy humans. There are increases in heart rate (HR), blood pressure (BP), and forearm blood flow (FBF) and concurrent increases in total body and forearm norepinephrine spillover (TB NE SO and FA NE SO), yet arterial and arm venous concentrations of epinephrine ([EPI]) remain unchanged. Infusion was 3H‐norepinephrine. This pattern exemplifies active attention without distress.
Figure 9. Figure 9. Cannon's denervated heart model demonstrating distress‐induced adrenal secretion. The rate of the denervated heart in a caged cat was recorded upon exposure of the animal to a dog, before and after bilateral adrenal inactivation. The virtual absence of tachycardia in the setting of inactivated adrenals indicated distress‐evoked adrenal release of a hormone into the bloodstream. Taken with permission from Cannon (29).
Figure 10. Figure 10. Estimates of rates of norepinephrine (NE) synthesis, vesicular recycling, release, neuronal, and extraneuronal uptake, and metabolism in cardiac sympathetic nerves in healthy humans and patients with congestive heart failure. Note that under resting conditions most of the turnover of NE is from net vesicular leakage, not release escaping reuptake. Cardiac NE spillover is influenced by both exocytotic release and neuronal reuptake.
Figure 11. Figure 11. Concept diagram depicting proposed mechanisms of takotsubo cardiopathy (stress cardiopathy). Taken with permission from Akashi et al. (3).
Figure 12. Figure 12. Plasma epinephrine (EPI), norepinephrine (NE), forearm vascular resistance (FVR), and mean arterial pressure (MAP) responses to tilt table testing in a patient with neurocardiogenic syncope. Note progressive decrease in FVR and increase in EPI prior to hypotension and syncope. Divergence of EPI from NE responses indicates sympathoadrenal imbalance.
Figure 13. Figure 13. Concept diagram for shifts in blood flow distribution associated with tilt‐induced syncope. The normal response to head‐up tilting includes sympathetically mediated skeletal muscle vasoconstriction, which counters decreased cardiac output and helps preserve cerebral blood flow. Skeletal muscle vasodilation combined with decreased cardiac output decreases brainstem perfusion, evoking syncope.
Figure 14. Figure 14. Meta‐analysis from of prospective studies examining cardiovascular reactivity to stress and subsequent cardiovascular status. Taken with permission from Chida and Steptoe (42).
Figure 15. Figure 15. Meta‐analysis from of prospective studies examining cardiovascular recovery from stress and subsequent cardiovascular status. Taken with permission Chida and Steptoe (42).
Figure 16. Figure 16. Adrenaline and ACTH responses to different stressors in humans, from a meta‐analysis of the literature. There is excellent agreement between adrenomedullary and adrenocortical activation. For instance, exposure to cold exerts little or no adrenomedullary or adrenocortical activation, whereas insulin‐induced hypoglycemia evokes large‐magnitude adrenomedullary and adrenocortical activation.


Figure 1. Original recordings of muscle sympathetic nerve activity (MSNA) and beat‐to‐beat arterial blood pressure during acute, laboratory‐based mental stress. Taken with permission from Wallin et al. (279).


Figure 2. Muscle sympathetic nerve activity (MSNA) responsiveness to mental stress was not correlated to arterial blood pressure responsiveness; DAP, diastolic arterial pressure. Taken with permission from Carter & Ray (39).


Figure 3. Mental stress increases forearm vascular conductance (FVC) without any change in forearm muscle sympathetic nerve activity (MSNA); VOP, venous occlusion plethysmography; DOPPLER, Doppler ultrasound technique; B, baseline; R, recovery. Modified with permission from Carter et al. (37).


Figure 4. Muscle sympathetic nerve activity correlates strongly with femoral venous (FV) plasma norepinephrine (NE) concentrations and spillover at rest, but not during mental stress elicited via Stroop's color word conflict test (CWT). Taken with permission from Hjemdahl et al. (133).


Figure 5. Skin sympathetic nerve activity (SSNA) responsiveness to mental stress was divergent in the tibial (T) and peroneal (P) nerves of hyperhidrosis patients. Taken with permission from Iwase et al. (137).


Figure 6. Skin sympathetic nerve activity (SSNA) responses to emotionally charged images from the International Affective Picture System (IAPS). Taken with permission from Brown et al. (24).


Figure 7. Panic disorder (PD) patient peripheral sympathetic neurons fire more often in a “multiple spike” pattern when compared to health controls. Taken with permission from Lambert et al. (172).


Figure 8. Hemodynamic and catecholamine responses to mental challenge (playing a video game) in healthy humans. There are increases in heart rate (HR), blood pressure (BP), and forearm blood flow (FBF) and concurrent increases in total body and forearm norepinephrine spillover (TB NE SO and FA NE SO), yet arterial and arm venous concentrations of epinephrine ([EPI]) remain unchanged. Infusion was 3H‐norepinephrine. This pattern exemplifies active attention without distress.


Figure 9. Cannon's denervated heart model demonstrating distress‐induced adrenal secretion. The rate of the denervated heart in a caged cat was recorded upon exposure of the animal to a dog, before and after bilateral adrenal inactivation. The virtual absence of tachycardia in the setting of inactivated adrenals indicated distress‐evoked adrenal release of a hormone into the bloodstream. Taken with permission from Cannon (29).


Figure 10. Estimates of rates of norepinephrine (NE) synthesis, vesicular recycling, release, neuronal, and extraneuronal uptake, and metabolism in cardiac sympathetic nerves in healthy humans and patients with congestive heart failure. Note that under resting conditions most of the turnover of NE is from net vesicular leakage, not release escaping reuptake. Cardiac NE spillover is influenced by both exocytotic release and neuronal reuptake.


Figure 11. Concept diagram depicting proposed mechanisms of takotsubo cardiopathy (stress cardiopathy). Taken with permission from Akashi et al. (3).


Figure 12. Plasma epinephrine (EPI), norepinephrine (NE), forearm vascular resistance (FVR), and mean arterial pressure (MAP) responses to tilt table testing in a patient with neurocardiogenic syncope. Note progressive decrease in FVR and increase in EPI prior to hypotension and syncope. Divergence of EPI from NE responses indicates sympathoadrenal imbalance.


Figure 13. Concept diagram for shifts in blood flow distribution associated with tilt‐induced syncope. The normal response to head‐up tilting includes sympathetically mediated skeletal muscle vasoconstriction, which counters decreased cardiac output and helps preserve cerebral blood flow. Skeletal muscle vasodilation combined with decreased cardiac output decreases brainstem perfusion, evoking syncope.


Figure 14. Meta‐analysis from of prospective studies examining cardiovascular reactivity to stress and subsequent cardiovascular status. Taken with permission from Chida and Steptoe (42).


Figure 15. Meta‐analysis from of prospective studies examining cardiovascular recovery from stress and subsequent cardiovascular status. Taken with permission Chida and Steptoe (42).


Figure 16. Adrenaline and ACTH responses to different stressors in humans, from a meta‐analysis of the literature. There is excellent agreement between adrenomedullary and adrenocortical activation. For instance, exposure to cold exerts little or no adrenomedullary or adrenocortical activation, whereas insulin‐induced hypoglycemia evokes large‐magnitude adrenomedullary and adrenocortical activation.
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Article Title: Sympathoneural and Adrenomedullary Responses to Mental Stress
 

How to Cite

Jason R. Carter, David S. Goldstein. Sympathoneural and Adrenomedullary Responses to Mental Stress. Compr Physiol 2014, 5: 119-146. doi: 10.1002/cphy.c140030