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1 Department of Physiology and the Centre for Neuroscience, University of Otago, Dunedin, New Zealand
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Abstract |
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 Top Abstract IntroductionMethodsResultsDiscussionReferences |
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30–35% by right atrial pacing. Baroreceptor regions were exposed to ramps of pressure (from 25 to 140 mmHg, at 0.5–1 mmHg s–1), generated by inflation and deflation of cuffs placed around the inferior vena cava and descending thoracic aorta. Response curves relating baroreceptor discharge to mean pressure were constructed and fitted with third-order polynomial expressions. To provide a measure of an effect of an increase in heart rate on the response curve in the region of the normal operating pressure, we calculated the position of the test response curve relative to the position of the control curve at 90 mmHg (
BP90). For the ADN, the activity of single fibres (presumptive myelinated fibres) was unaffected by increasing heart rate (BP90
=
+0.1 ± 1.0 mmHg), while single fibres in the CSN showed a small increase in activity (BP90
=
–1.5 ± 0.3 mmHg). In multifibre preparations there was a small increase in activity that may be attributable to additional activity in unmyelinated fibres (ADN, BP90
=
–3.4 ± 1.2 mmHg; CSN, BP90
=
–5.2 ± 0.9 mmHg). We conclude that the mean discharge of arterial baroreceptors remains a reliable index of mean arterial pressure in the presence of substantial changes in heart rate.
(Received 15 March 2006;
accepted after revision 29 March 2006; first published online 1 June 2006)
Corresponding author C. P. Bolter: Department of Physiology, School of Medical Sciences, University of Otago, PO Box 913, Dunedin, New Zealand. Email: chris.bolter{at}otago.ac.nz
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Introduction |
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Whether pulse frequency can modulate the mean firing rate of baroreceptor afferent fibres has been a longstanding question. Several early studies found that mean baroreceptor activity was not dependent on pulse frequency (Angell James, 1971; Arndt et al. 1975; Brown et al. 1978). However, in each of these studies a sinusoidal pressure wave rather than the naturally occurring pulse waveform was used to examine the influence of pulse frequency. Attention was drawn to the marked differences in both peak rate of pressure development (dP/dt) and duration of systolic pressure rise of the natural pulse compared with a symmetrical sinusoidal pulse by Abboud & Chapleau (1988). They suggested that alterations in the frequency of the natural asymmetric pulse would alter mean baroreceptor activity, and tested their hypothesis by examining the activity of canine carotid sinus single baroreceptor afferent fibres. The carotid sinus was exposed to mechanically generated sinusoidal and ‘natural’ pressure waveforms, or to the spontaneously generated natural pressure wave. Using both asymmetric waveforms, they found that at a given value of systolic arterial pressure the mean discharge of arterial baroreceptors was greater at a higher pulse frequency, and concluded that pulse frequency was an important modulator of the mean discharge of single carotid sinus baroreceptor afferent fibres.
The modulation of baroreceptor activity by pulse frequency could play an important role in the regulation of blood pressure. While the results of Abboud & Chapleau (1988) suggest that this might be the case, we really need to know whether significant modulation of baroreceptor discharge is also evident at equivalent values of mean arterial pressure. Consequently, we have re-examined the question of whether changes in heart rate significantly influence the mean activity in baroreceptor afferent fibres. Experiments were performed on anaesthetized rabbits, with recordings made from both multifibre (whole nerve) and single fibre preparations of the carotid sinus and aortic depressor nerves (CSN and ADN). The baroreceptor regions were exposed to the naturally occurring pulse wave. We have recorded baroreceptor activity over a large range of arterial pressure, plotted ‘response curves’, and fitted these curves mathematically to provide a reliable index of baroreceptor activity in the normal operating range.
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Methods |
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Experiments were performed on New Zealand albino rabbits of either sex, weighing 2.2–5.0 kg. They were anaesthetized with sodium pentobarbitone (30–40 mg kg–1; Nembutal, Abbott, Abbott Park, IL, USA) administered through a marginal ear vein. To maintain an adequate level of anaesthesia, further anaesthetic (5–10 mg kg–1) was administered as required. Colonic temperature was kept between 37.0 and 38.0°C by a thermostatically controlled heating blanket. At the conclusion of the experiment, the animal was killed with an overdose of sodium pentobarbitone.
Experimental preparation
The trachea was cannulated and the animal ventilated mechanically with room air. Catheters were placed in a femoral artery for monitoring arterial blood pressure and in a femoral vein for drug and fluid administration.
Experiments were performed on either the left aortic depressor nerve (ADN) or on the right carotid sinus nerve (CSN). To prepare a nerve, a mid-line incision was made in the skin, extending from the chin to the top of the sternum, and the edges of the skin were clamped into a 15 cm diameter frame to provide a wide exposure. The ADN was separated from surrounding tissue, but left intact. The CSN was separated from surrounding tissue and cut at its junction with the glossopharyngeal nerve. In experiments on aortic baroreceptors, aortic pressure was measured from a catheter advanced to the aortic arch from the brachial artery. In experiments on carotid baroreceptors, carotid bifurcation pressure was measured from a catheter inserted into a branch of the external carotid artery, with its tip positioned just rostral to the carotid bifurcation.
The chest was opened at the left and right fourth intercostal spaces. Through these incisions, 5 mm diameter perivascular cuffs (In Vivo Metric, Healdsburg, CA, USA) were secured around the descending thoracic aorta the inferior vena cava. Lung inflation was maintained by applying an end-expiratory pressure of 3–5 cmH2O.
Cardiac pacing
A catheter with a bipolar platinum electrode at its tip was inserted into a branch of the right external jugular vein and advanced until it lodged in the right atrium. Cardiac rhythm was captured using square-wave electrical pulses of 5–10 V and 1.0 ms duration (Grass SD9, Grass Instruments Co., Quincy, MA, USA). Heart rate could be driven by pacing to a value of approximately 100 beats min–1 higher than the spontaneous value without development of obvious arrhythmia or pulsus alternans.
Recording baroreceptor activity
To obtain recordings of multifibre activity, the ADN or CSN was placed on a pair of platinum electrodes and embedded in a fast-curing silicone gel. To obtain recordings from single baroreceptor afferent fibres, the nerve was cut centrally, the sheath removed, and the nerve split into small filaments. Recordings were made from filaments in which action potentials from one fibre could be clearly discriminated. The filament was placed over a single electrode, and the indifferent electrode was earthed to the surrounding tissue through a fine cotton thread.
Signals from nerve preparations were amplified and filtered (multifibre preparations: high-pass 100 Hz, low-pass 10 kHz; single fibre preparations: high-pass 100 Hz, low-pass 3 kHz) using a differential preamplifier (model P15D, Grass Instruments Co.) and oscilloscope preamplifier (5A22N, Tektronix, Beaverton, OR, USA).
Arterial pressure ramps
Inflation and deflation of the cuff around the inferior vena cava, followed by inflation of the cuff around the aorta, generated a pressure ramp that rose from 25 to 140 mmHg, at 0.5–1.0 mmHg s–1. Both the carotid bifurcation and the aortic arch were exposed to the pressure ramp produced by this manoeuvre. After the ramp had been completed, the aortic cuff was deflated, and arterial pressure was allowed to return to the control level.
Data acquisition
Pressure at the aortic arch and carotid bifurcation was measured using Statham P23DC pressure transducers (Hato Rey, Puerto Rico). These were connected to a Grass bridge amplifier (model 7P1DE), and the mean pressure was derived by low-pass filtering. Heart rate was monitored using an instantaneous ratemeter (Narco-Bio-systems biotachometer coupler, type 7302, Austin, TX, USA) that was triggered by the arterial pulse.
Analogue signals of nerve activity, blood pressure and heart rate were digitized (Vetter PCM, model 3000A, Rebersburg, PA, USA) and stored on videotape. Subsequently the tape was played back, and the signals were processed to generate the Chart file used for data analysis (Chart 3.4, ADInstruments, Castle Hill, NSW, Australia). Action potential frequency was obtained by passing the electroneurogram through a custom-made discriminator and counter. For multifibre activity, the threshold of the discriminator was set just above the noise level that was recorded either at the conclusion of the experiment after the nerve had been cut peripherally, or when nerve activity ceased temporarily following a sharp drop in pressure. Action potentials were counted in 0.2 s bins. This system had a linear response to over 2000 Hz.
Experimental protocol
Each experiment comprised a number of pressure ramps recorded under control conditions (control ramps) that alternated with ramps recorded while the heart rate was elevated by pacing (test ramps). There was a 5 min interval between each ramp. Pacing started 1 min before the test ramp was produced and concluded at the end of the ramp.
In most multifibre preparations, four control and three test ramps were completed. Experiments on multifibre preparations always started and finished with a control ramp. In experiments examining single afferent fibre activity, data collection began once a single fibre had been isolated. In most instances, a data set consisted of a single test ramp preceded and followed by a control ramp.
In a number of experiments on both single and multifibre preparations of the ADN, control pressure ramps were applied repeatedly at 5 min intervals.
Data analysis
Many previous studies have used the value of the threshold pressure at the onset of nerve activity to quantify changes in the relationship between baroreceptor activity and arterial pressure. However, the threshold pressure often lies well below an animal's normal operating pressure and a change in its value may not accurately reflect an alteration in the pressure–activity relationship in the region of the operating pressure. In our analysis, the level of baroreceptor activity recorded at a mean arterial pressure of 90 mmHg during control ramps has been used as the reference point.
The influence of a change in heart rate on nerve activity was determined as follows. A response curve relating baroreceptor activity to pressure was constructed for every ramp, and third-order polynomial equations were fitted. The polynomial expressions fitted the raw data well, especially within ± 10 mmHg of the reference pressure (90 mmHg); the square of the correlation coefficient, R2 exceeded 0.99 over the full pressure range for all individual response curves. These equations were then used to generate a single mean response curve representing the control and test ramps in each preparation. From these curves we determined the pressure in the test ramp that generated the level of nerve activity that was observed at 90 mmHg in the control ramp. We termed the difference between this pressure and 90 mmHg theBP90. A positive value forBP90 represents a right shift of the response curve under test conditions, and vice versa.
Statistical analysis
Data are presented as group means ± 1 standard deviation. Differences between mean values were examined using the Wilcoxon signed ranks test.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Recordings were made from eight preparations of the ADN and seven of the CSN. In preparations of both nerves, the increase in heart rate achieved by pacing was approximately 100 beats min–1 (Table 1). Pacing did not result in a change in baseline mean arterial pressure (MAP; Table 1). Figure 1 presents raw data from seven pressure ramps performed in a single preparation of the ADN. Nerve activity is plotted for 2.5 mmHg increments in aortic pressure. At pressures above 60 mmHg, pacing at the higher rate increased nerve activity, resulting in a left shift of the response curve.
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50 mmHg, and the relationship between activity and pressure took on a sigmoidal appearance. In contrast, activity in the CSN (Fig. 2B) increased monotonically, with the steepest part of the response curve occurring at lower pressures. Pacing the heart at a higher rate resulted in an increase in the activity in both the ADN and the CSN. This effect was more evident at the higher pressures. There was a similar and significant leftward shift in the response curves of both the ADN and the CSN at the higher heart rate (Table 1).
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In 11 multifibre preparations of the ADN, reproducible response curves were generated by seven repeated applications of a pressure ramp. The calculatedBP90 (comparing 4 odd-numbered versus 3 even-numbered ramps) was +0.7 ± 0.9 mmHg (P
= 0.55).
Single fibre preparations
We recorded the effect of an increase in heart rate on the activity of 14 fibres from the ADN (5 animals) and 15 fibres from the CSN (5 animals). Conduction velocity was not measured, but a high discharge frequency and low pressure threshold of these fibres suggested that they were mainly A fibres (31). Only one fibre from the ADN and one fibre from the CSN had a maximum frequency of less than 40 action potentials s–1. Pacing increased heart rate by 85–90 beats min–1, without altering MAP (Table 1). The increase in heart rate achieved by atrial pacing in the single fibre preparations was slightly, but significantly, less than that obtained in the multifibre preparations (P < 0.01).
For single fibres from the ADN, there was no shift in the response curve in response to pacing (Figs 3–5). There was a small shift in the response curve for single fibres from the CSN, with a left shift recorded in 13 of the 15 fibres examined (Figs 3 and 5). Response curves for single fibres from the ADN and CSN were similar in form and threshold to those recorded from multifibre preparations of the same nerve. Single fibres dissected from the CSN were most often silent below their threshold pressure (13 out of 15 fibres), while 7 out of 14 fibres from the ADN fired with regular pulse-synchronous bursts at subthreshold pressures (Fig. 4). In the preparations of the ADN, pacing resulted in a fall in pulse pressure that measured 2.9 ± 1.4 mmHg at a mean aortic pressure of 90 mmHg. In the preparations of the CSN, the effect of pacing was a reduction in pulse pressure of 3.6 ± 2.0 mmHg at a mean carotid bifurcation pressure of 90 mmHg.
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BP90
=
+1.8 ± 1.6 mmHg, P
= 0.24, n
= 9). |
Discussion |
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90 mmHg in multifibre recordings from both the CSN and the ADN. In contrast, the response curves obtained from single nerve fibre preparations from both nerves were essentially unaltered by pacing. The single baroreceptor afferent fibres that we sampled had a low threshold pressure and high discharge frequency, indicating that they were most probably myelinated fibres (Thorén & Jones, 1977; Yao & Thorén, 1983). Since the mean discharge of the single fibre baroreceptor afferents was essentially unaffected by the increase in heart rate, cyclic discharge must have varied inversely with the pacing-induced increase in heart rate. The samples of firing pattern illustrated in Fig. 3 show that, for both the ADN and the CSN, the reduction in cyclic discharge at the higher heart rate may be attributable primarily to a reduction in diastolic activity. The duration of diastole was reduced at the higher heart rate, resulting in an increase in the rate of fall of pressure in diastole (–dP/dt) that was accompanied by a rapid cessation of baroreceptor firing. These findings contrast with those of Abboud & Chapleau (1988), who reported a significant increase in canine carotid baroreceptor activity in response to an increase in pulse frequency. It seems unlikely that the difference between the two sets of results can be attributed to a species difference. One possible source for the divergent findings may be the manner in which the data have been analysed. We have referred our measures of nerve activity, both single and multifibre, to the mean arterial pressure at the receptor location. In contrast, in experiments on carotid baroreceptors exposed to the natural pulse, Abboud and Chapleau referred nerve activity to systolic arterial pressure. Their analysis (Abboud & Chapleau, 1988; their Table 3) shows that when mean heart rate was increased from 90 to 143 beats min–1, mean baroreceptor activity increased by an amount equivalent to that which would have accompanied a 7 mmHg increase in systolic arterial pressure. We have re-examined their data by using mean arterial pressure as the independent variable (mean arterial pressure was estimated from values for pulse and systolic pressure provided by Abboud & Chapleau, 1988; their Fig. 6 and Table 3). When the effect of heart rate on mean baroreceptor activity is compared at the equivalent mean arterial pressure, no effect is evident in their data either.
In our experiments, pacing reduced the pulse pressure by 3–4 mmHg at a mean pressure of 90 mmHg in the aortic arch and carotid bifurcation, the reference pressure used in our analysis. This fall in pulse pressure would be associated with a small decrease in systolic pressure (2–3 mmHg). If we plotted the relationship between single fibre activity and systolic pressure, the curve for the paced condition would lie above and to the left of the control curve. This effect of pacing on the relationship between single fibre baroreceptor activity and systolic pressure is similar to that reported by Abboud & Chapleau (1988). We suggest that the effect of heart rate on baroreceptor activity reported by Abboud and Chapleau was a consequence of a difference in the pulse pressure at different heart rates and the use of systolic pressure as the independent variable.
Although a change in heart rate had no effect on the mean discharge of our single fibre preparations, it did alter the discharge rate of multifibre preparations. What can account for this effect? Angell James (1971) has suggested that an increase in heart rate might be expected to increase the chance of firing in unmyelinated afferents, and concluded that an increase heart rate would result in a small increase in total impulse activity in multifibre preparations. Is this a reasonable explanation for the responses obtained in our multifibre recordings? In the rabbit, the aortic depressor nerve is composed almost entirely of afferent fibres coupled to baroreceptor endings, while the afferent fibre population of the carotid sinus nerve is connected to both chemoreceptors and baroreceptors (Qu & Stuesse, 1991). The raw electroneurogram of the CSN exhibited a distinct discharge during systole, often with total silence during diastole. Also, a period of total silence occurred briefly when pressure was reduced abruptly at the start of a pressure ramp, or when pressure fell at the conclusion of a ramp. Therefore, we conclude that our recordings of CSN multifibre activity represent primarily the discharge of the carotid baroreceptors. Since the ADN and CSN multifibre preparations responded similarly to an increase in heart rate, we conclude that the behaviour of unmyelinated baroreceptor afferent activity present in the multifibre discharge of both the ADN and CSN, but not observed as single fibre activity, may account for the responses shown by the multifibre preparations.
In our study, we treated mean activity recorded from baroreceptor afferent fibres as a measure of information about MAP, as conveyed to the brainstem structures involved in arterial baroreflex regulation. This interpretation suggests that the afferent signal the brain receives about the value of mean arterial pressure is robust in the face of alterations in heart rate. In a study on the effect of heart rate on canine left atrial B receptors, Zucker & Gilmore (1976) reported a similar robust relationship between the mean activity of the atrial receptors and atrial pressure in the face of large changes in heart rate. At the same time, they noted that the number of action potentials per cardiac cycle and the peak discharge frequency declined when heart rate was increased, and suggested that these characteristics of the atrial discharge may be important for the generation of certain reflex effects. It is also possible that alterations in the frequency of arrival of the bursts of activity, consequent to a change in heart rate, may alter the operation of the reflex independent of any change in mean activity. The regular bursting nature of the baroreceptor input appears to be a critical determinant of the control of the neural output (sympathetic activity) of the baroreflex arc. The bursting input produces facilitation of the central neurones as a consequence of an alternation between afferent activity during systole and silence during diastole (Chapleau & Abboud, 1987; Mifflin & Felder, 1988; Rogers et al. 1993). An alteration in the frequency at which the bursting discharge appears at the central neurones may alter the relative proportions of the periods of systolic active input and diastolic silence, as well as the interburst interval.
There are few reports on the effect of a change in heart rate on the open-loop baroreflex control of the circulation, or on its efferent nervous input. Using vascularly isolated preparations of the canine carotid sinus, Chapleau et al. (1989) found that increases in pulse frequency produced weaker reflex effects in efferent sympathetic nervous activity, and concluded that this was a consequence of a reduction in diastolic silence. They also suggested that subtle alterations in fibre recruitment or in the distribution of activity within a burst, for example an increase in peak discharge frequency, may also affect the central responses to baroreceptor input (Chapleau et al. 1989). We are not aware of any studies that have examined these possibilities in detail, in particular not with the use of a natural or physiologically generated signal. A recent study suggests that open-loop gain of the arterial baroreflex in the rabbit may be unaffected by substantial changes in pulse frequency and amplitude. Kawada et al. (2002) used data on the rabbit carotid baroreflex to model the ‘neural arc’ of the arterial baroreflex. The open-loop gain of the neural arc remained stable over a heart rate range of 0.8–6.0 Hz, provided that pulse pressure was less than about 50 mmHg. Our observations are consistent with their conclusions; one might anticipate small variations in the operating point of the reflex to occur when heart rate moves within the range of 5.0–6.5 Hz, but this should not be accompanied by a change in open-loop gain.
We consider that mean arterial pressure, rather than systolic or diastolic pressure, is the controlled and regulated variable of the arterial baroreflex. As such, it appears appropriate to treat mean arterial pressure as the independent variable when examining baroreceptor activity or baroreflex function. However, both the mean and the systolic and diastolic pressures (estimated) have been used as the independent variable in recent studies on the arterial baroreflex in humans. While some authors report baroreflex regulation of heart rate using mean carotid sinus pressure as the independent variable (Smith et al. 2003; Matsukawa et al. 2006), others use systolic carotid arterial pressure (Halliwill & Minson, 2002), because heart rate correlates closely with systolic pressure but not with diastolic pressure (Sundlöf & Wallin, 1977; Rudas et al. 1999). In another study, the authors plotted the relationship between heart period and systolic carotid sinus pressure (Umehara et al. 2006). In order to compare their results with other studies, Linnarsson et al. (2006) analysed their data twice: once as the relationship between heart rate and mean arterial pressure, and then as the relationship beween pulse interval and systolic pressure. In two separate studies that investigated the baroreflex regulation of muscle sympathetic nerve activity, diastolic pressure was treated as the independent variable (Halliwill & Minson, 2002; Ichinose et al. 2004). This approach was used because changes in sympathetic activity correlate closely with diastolic pressure but not with systolic pressure (Sundlöf & Wallin, 1977; Rudas et al. 1999). In contrast, Fadel et al. (2001) examined the baroreflex control of muscle sympathetic activity using mean pressure as the independent variable. It appears that we need to consider carefully the criteria for choosing the independent variable for the analysis of baroreflex control since the mean, the systolic and the diastolic pressure have been used in this role in these examples of recent studies. Is either the strength of a correlation or the functional relevance of a relationship an appropriate criterion? What approach should be taken if two criteria are mutually exclusive?
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References |
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and •) and a single ramp during pacing (