Baroreflex control of muscle sympathetic nerve activity is attenuated in the elderly

doi:10.1016/S0165-1838(98)00128-3

Journal of the Autonomic Nervous System

Volume 73, Issues 2–3, 10 November 1998, Pages 182-185

Journal of the Auton...

https://doi.org/10.1016/S0165-1838(98)00128-3 Get rights and content

Abstract

To determine whether the baroreflex control of sympathetic nerve activity is attenuated in the elderly, muscle sympathetic nerve activity (MSNA) from the tibial nerve was monitored using microneurography, and heart rate and blood pressure were recorded during the depressor (phase II) or pressor (phase IV) period to Valsalva's maneuver in 10 younger subjects and 7 aged subjects. The baroreflex slope for heart rate showed attenuation in the aged subjects during the pressor phase but not during the depressor phase, the baroreflex slope for MSNA was also attenuated in the aged subjects during the pressor and tended to be attenuated during the depressor phases. These data suggest impaired baroreflex function for both heart rate and sympathetic nerve activity in the elderly.

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Cited by (44)

Stress and the “extended” autonomic system
2021, Autonomic Neuroscience: Basic and Clinical
Citation Excerpt :
Baroreflex sensitivity, and therefore the ability to keep blood pressure within bounds, declines with age in a manner associated with hypertension (Bristow et al., 1969). The rate of pulse-synchronous bursts of skeletal muscle sympathetic nerve traffic increases with aging (Sundlof and Wallin, 1978); however, arterial baroreflex control of muscle sympathetic nerve traffic (Matsukawa et al., 1998) and of cardiovagal outflow are decreased in the elderly (Bristow et al., 1969). All forms of distress increase blood pressure and inhibit baroreflex functions (Goldstein, 1983).
This review updates three key concepts of autonomic neuroscience—stress, the autonomic nervous system (ANS), and homeostasis. Hans Selye popularized stress as a scientific idea. He defined stress variously as a stereotyped response pattern, a state that evokes this pattern, or a stimulus that evokes the state. According to the “homeostat” theory stress is a condition where a comparator senses a discrepancy between sensed afferent input and a response algorithm, the integrated error signal eliciting specific patterns of altered effector outflows. Scientific advances since Langley's definition of the ANS have incited the proposal here of the “extended autonomic system,” or EAS, for three reasons. (1) Several neuroendocrine systems are bound inextricably to Langley's ANS. The first to be described, by Cannon in the early 1900s, involves the hormone adrenaline, the main effector chemical of the sympathetic adrenergic system. Other neuroendocrine systems are the hypothalamic-pituitary-adrenocortical system, the arginine vasopressin system, and the renin-angiotensin-aldosterone system. (2) An evolving body of research links the ANS complexly with inflammatory/immune systems, including vagal anti-inflammatory and catecholamine-related inflammasomal components. (3) A hierarchical network of brain centers (the central autonomic network, CAN) regulates ANS outflows. Embedded within the CAN is the central stress system conceptualized by Chrousos and Gold. According to the allostasis concept, homeostatic input-output curves can be altered in an anticipatory, feed-forward manner; and prolonged or inappropriate allostatic adjustments increase wear-and-tear (allostatic load), resulting in chronic, stress-related, multi-system disorders. This review concludes with sections on clinical and therapeutic implications of the updated concepts offered here.
Applanation tonometry for evaluation of the haemodynamic response to the active orthostatic test
2017, Artery Research
Citation Excerpt :
This finding is in harmony with the reported inverse correlation between carotid artery stiffness and sympathetic baroreflex in the elderly.46 Our supposition for reduced arterial baroreflex efficiency and decreased sympathetic efferent discharge to the resistive arterioles in our 60-YO individuals is supported by data that showed impaired baroreflex and reduced muscle sympathetic nerve activity through direct recording in the elderly.47 We analysed HRV for non-invasive evaluation of the autonomic influences on the cardiovascular system in response to the active orthostatic test (Table 2, Fig. 5).
Our study was aimed at the assessment of the age-specific hemodynamic response to the active orthostatic test (OT).
Two groups (60-Y/O and 20-Y/O) were subjected to OT (three 5-minute periods: baseline supine, upright standing, recovery supine). Continuous electrocardiogram was recorded and heart rate variability (HRV) analysed. At the end of each period pulse wave analysis was performed (Sphygmocor, AtCor Medical).
We observed significantly higher radial and central systolic and pulse pressures in the adults at baseline. We found out reduced efficiency of the hemodynamic compensatory response to orthostasis in the 60-Y/O group: mild heart rate increase (75 ± 2 vs. 88 ± 3 beats per minute); moderate aortic systolic pressure reduction (124 ± 6 to 119 ± 5 vs. 99 ± 2 to 101 ± 3 mm Hg); considerable aortic pulse pressure decrease (47 ± 4 to 38 ± 3 vs. 27 ± 2 to 22 ± 2 mm Hg); absence of diastolic pressure elevation. The adults showed significantly higher baseline augmentation indices (AIx); the young responded to the upright position with noticeable reduction of AIx most probably resulting from the pronounced tachycardia and the consequent delayed timing of pulse wave return. HRV data showed milder sympathetic activation in the 60-Y/O individuals in response to OT as compared to the 20-Y/O.
Pulse wave analysis provided new knowledge concerning the age-related hemodynamic response pattern to active orthostasis. We believe the underlying mechanism was the ‘physiological’ arterial stiffening with aging and the ensuing reduced arterial baroreflex sensitivity. HRV data for lesser sympathetic activation in response to the orthostatic challenge in the 60-Y/O group supported this assumption.
New insights into the effects of age and sex on arterial baroreflex function at rest and during dynamic exercise in humans
2012, Autonomic Neuroscience: Basic and Clinical
Citation Excerpt :
Aging is associated with a plethora of alterations in cardiovascular morphology, function and regulation (Lakatta, 1993). With increased age, a decrease in cardiac parasympathetic nerve activity (Davies, 1975; Stratton et al., 2003) and a reduction in cardiac ABR sensitivity (Ebert et al., 1992; Fisher et al., 2007; Gribbin et al., 1971; Matsukawa et al., 1996, 1998) have been consistently identified. Although increases in resting SNA in older individuals are also well characterized (Hogikyan and Supiano, 1994; Seals and Esler, 2000), whether aging modifies ABR regulation of vasoconstrictor muscle SNA remains equivocal, with impaired, preserved, and enhanced responsiveness reported in older individuals (Davy et al., 1998; Ebert et al., 1992; Jones et al., 2001; Matsukawa et al., 1996, 1998; Studinger et al., 2009).
The arterial baroreflex (ABR) performs an important role in regulating blood pressure (BP) both at rest and during exercise, by carefully orchestrating autonomic neural activity to the heart and blood vessels. Reduced ABR sensitivity (i.e., gain) has been associated with increased cardiovascular risk, cardiac electrical instability and orthostatic intolerance, while ‘normal’ ABR function during exercise is important for ensuring an appropriate cardiovascular response is elicited. Previous studies examining the influence of age and sex on resting ABR function in humans have primarily used pharmacological methods (e.g., modified Oxford technique) to change BP and alter baroreceptor input. With this approach only reflex control of heart rate and sympathetic nerve activity may be evaluated, and as such the influence of age and sex on ABR control of BP per se remains incompletely understood. Furthermore, the majority of previous studies examining ABR function during exercise have principally assessed young men. Whether these findings can be extrapolated to young women or older men and women remains unclear. Recently the potential for age and sex to modulate the integrative neural control of the cardiovascular system is becoming appreciated. This review article will provide a detailed update of such recent advances into our understanding of the effects of age and sex on ABR control of BP both at rest and during dynamic exercise in humans.
Short-term sympathetic baroreflex sensitivity increases at lower blood pressures
2008, Clinical Neurophysiology
Citation Excerpt :
This difference in baroreflex gain between the spontaneous and infusion methods might be explained by the fact that these methods study different changes in time of blood pressure and the related MSNA. Sympathetic activity responds not only to the level of diastolic pressure, but also to the way the pressure changes in time, for instance whether it increases or decreases (Sundlöf and Wallin, 1978; Matsukawa et al., 1998). Some authors acknowledge the effect of time by distinguishing between the ‘initial reflex’ and the ‘sustained baroreflex response’ (Davy et al., 1998b).
Sympathetic baroreflex sensitivity (symBRS) can be defined as the maximum sensitivity of muscle sympathetic nerve activity (MSNA) to changes in arterial blood pressure. This sensitivity is the slope of the linear middle part of the sigmoid curve that relates blood pressure to MSNA. SymBRS is known to vary with conditions, for instance during cold pressor testing. We investigated whether symBRS is affected by infusions of phenylephrine and nitroprusside.
In 10 healthy subjects, vasoactive infusions were varied in slow steps, as customary in protocols to determine ‘graded infusion symBRS’ (symBRS_inf). During each step, symBRS was estimated from spontaneous beat-to-beat fluctuations (symBRS_sp). As a secondary goal, symBRS_inf was compared to the symBRS_sp without infusions.
The symBRS_sp for MSNA burst area varied with infusions, augmenting with decreasing blood pressure, however the symBRS_sp for burst occurrence was not affected. There were large differences between symBRS_inf and symBRS_sp at rest.
symBRS_sp varies systematically with infusions during a symBRS_inf protocol. This denotes a fundamental difference between these methods.
The relationship between ‘slow’ infusion effects (symBRS_inf) and changes in symBRS_sp is elucidated. The mathematical model that describes this relationship can also explain the increase of symBRS found with other sympathoexcitatory stimuli.
Orthostatic Hypotension-Related Hospitalizations in the United States
2007, American Journal of Medicine
Citation Excerpt :
Aging is associated with physiological changes that may predispose to orthostatic problems. For instance, there is a loss of baroreflex responsiveness,21,22 reduced cardiac compliance,23and attenuation of the vestibular sympathetic reflex.24 Therefore, the association between age and orthostatic hypotension has plausible physiological mechanisms.
Orthostatic hypotension has been commonly described in elderly persons and is associated with an increased risk of falls, syncope, and cerebrovascular events. Nevertheless, the precise burden of this condition in the US is currently unknown.
We analyzed discharge data from the Nationwide Inpatient Sample to identify orthostatic hypotension-related hospitalizations and associated comorbidities after excluding acute causes of this condition. National hospitalization rates were estimated using US census population estimates, and the medical conditions most frequently associated with orthostatic hypotension were assessed.
In 2004, there were an estimated 80,095 orthostatic hypotension-related hospitalizations, yielding an overall rate of 36 (95% confidence interval, 34 to 38) hospitalizations per 100,000 US adults. Orthostatic hypotension was the primary diagnosis in 35% of these hospitalizations. The number of orthostatic hypotension-related hospitalizations increased steadily with age, and patients aged 75 years or older had the highest annual hospitalization rate, 233 per 100,000 (95% confidence interval, 217 to 249). The median length of hospital stay was 3 days (IQR 2-6) and the overall in-hospital mortality was 0.9%. Caucasian males were most likely to be hospitalized with orthostatic hypotension. Syncope was the most common comorbid condition reported among orthostatic hypotension patients.
Orthostatic hypotension is a relatively common condition among hospitalized US elderly patients. In light of the progressive aging of the US population, the contribution of orthostatic hypotension to morbidity and mortality is likely to increase, and deserves further scrutiny.
Microneurography as a tool in clinical neurophysiology to investigate peripheral neural traffic in humans
2006, Clinical Neurophysiology
Microneurography is a method using metal microelectrodes to investigate directly identified neural traffic in myelinated as well as unmyelinated efferent and afferent nerves leading to and coming from muscle and skin in human peripheral nerves in situ. The present paper reviews how this technique has been used in clinical neurophysiology to elucidate the neural mechanisms of autonomic regulation, motor control and sensory functions in humans under physiological and pathological conditions.
Microneurography is particularly important to investigate efferent and afferent neural traffic in unmyelinated C fibers. The recording of efferent discharges in postganglionic sympathetic C efferent fibers innervating muscle and skin (muscle sympathetic nerve activity; MSNA and skin sympathetic nerve activity; SSNA) provides direct information about neural control of autonomic effector organs including blood vessels and sweat glands. Sympathetic microneurography has become a potent tool to reveal neural functions and dysfunctions concerning blood pressure control and thermoregulation. This recording has been used not only in wake conditions but also in sleep to investigate changes in sympathetic neural traffic during sleep and sleep-related events such as sleep apnea. The same recording was also successfully carried out by astronauts during spaceflight.
Recordings of afferent discharges from muscle mechanoreceptors have been used to understand the mechanisms of motor control. Muscle spindle afferent information is particularly important for the control of fine precise movements. It may also play important roles to predict behavior outcomes during learning of a motor task.
Recordings of discharges in myelinated afferent fibers from skin mechanoreceptors have provided not only objective information about mechanoreceptive cutaneous sensation but also the roles of these signals in fine motor control. Unmyelinated mechanoreceptive afferent discharges from hairy skin seem to be important to convey cutaneous sensation to the central structures related to emotion. Recordings of afferent discharges in thin myelinated and unmyelinated fibers from nociceptors in muscle and skin have been used to provide information concerning pain. Recordings of afferent discharges of different types of cutaneous C-nociceptors identified by marking method have become an important tool to reveal the neural mechanisms of cutaneous sensations such as an itch.
No direct microneurographic evidence has been so far proved regarding the effects of sympathoexcitation on sensitization of muscle and skin sensory receptors at least in healthy humans.

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Short communicationBaroreflex control of muscle sympathetic nerve activity is attenuated in the elderly

Abstract

J. Auton. Nerv. Syst.

J. Auton. Nerv. Syst.

Electroencephalogr. Clin. Neurophysiol.

Effect of posture on blood pressure in the elderly

Br. Heart J.

A modified method of quantifying the carotid baroreceptor-heart rate reflex in man: the effect of age and blood pressure

Clin. Sci.

Effects of aging on baroreflex regulation of sympathetic activity in humans

Am. J. Physiol.

Effect of age and high blood pressure on baroreflex sensitivity in man

Circ. Res.

Arterial baroreflexes in renal hypertensive rabbits

Circ. Res.

Short communication
Baroreflex control of muscle sympathetic nerve activity is attenuated in the elderly