Firing properties of single vasoconstrictor neurones in human subjects with high levels of muscle sympathetic activity.
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1. Single-unit recordings were made from 19 postganglionic muscle vasoconstrictor axons via tungsten microelectrodes in the peroneal nerve in seven healthy subjects with many multi-unit sympathetic discharges at rest ('high group', 75 +/- 5 multi-unit bursts per 100 heart beats, mean +/- s.e.m.). The results were compared with previous data from 14 units in subjects with 21 +/- 2 multi-unit bursts per 100 heart beats ('low group'). 2. In the 'high group' the units fired spontaneously in 35 +/- 4 % of all cardiac intervals. One unit only ever fired once per cardiac interval, 14 units (74 %) generated maximally two to three spikes, and four units (21 %) up to four to five spikes. Of those cardiac intervals in which a unit fired, a single spike occurred in 78 %, two spikes in 18 %, three spikes in 4 % and four spikes in less than 1 % of cardiac intervals. Measured as the inverse of all interspike intervals, the mean rate was 0.33 +/- 0.04 Hz and the mean intraburst frequency 22.2 +/- 1.6 Hz. Most results were similar to those in the 'low group', but in the 'low group' heart rate was higher (64.5 vs. 50.4 beats min-1) and mean firing frequency was higher (0.49 +/- 0.06 Hz). 3. During increases of multi-unit burst activity evoked by sustained inspiratory-capacity apnoea the firing probability of nine units in the 'high group' increased from 33 +/- 6 to 56 +/- 3 % of the cardiac intervals. Simultaneously, the incidence of single spikes decreased and the incidence of multiple spikes per cardiac interval increased, resulting in an increase of mean firing frequency from 0. 23 +/- 0.04 Hz at rest to 1.04 +/- 0.14 Hz during the apnoea. 4. We conclude that single muscle vasoconstrictor neurones usually fire only a solitary spike during sympathetic bursts both in subjects with a high and in subjects with a low number of bursts at rest. Presumably, differences in the numbers of bursts are due mainly to differences in firing probability and recruitment of sympathetic fibres. During acute increases of multi-unit activity, both increases in discharge frequency and recruitment of additional neurones contribute to the increased intensity of an individual sympathetic burst. (+info)
Augmented sympathetic activation during short-term hypoxia and high-altitude exposure in subjects susceptible to high-altitude pulmonary edema.
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BACKGROUND: Pulmonary hypertension is a hallmark of high-altitude pulmonary edema and may contribute to its pathogenesis. Cardiovascular adjustments to hypoxia are mediated, at least in part, by the sympathetic nervous system, and sympathetic activation promotes pulmonary vasoconstriction and alveolar fluid flooding in experimental animals. METHODS AND RESULTS: We measured sympathetic nerve activity (using intraneural microelectrodes) in 8 mountaineers susceptible to high-altitude pulmonary edema and 7 mountaineers resistant to this condition during short-term hypoxic breathing at low altitude and at rest at a high-altitude laboratory (4559 m). We also measured systolic pulmonary artery pressure to examine the relationship between sympathetic activation and pulmonary vasoconstriction. In subjects prone to pulmonary edema, short-term hypoxic breathing at low altitude evoked comparable hypoxemia but a 2- to 3-times-larger increase in the rate of the sympathetic nerve discharge than in subjects resistant to edema (P<0.001). At high altitude, in subjects prone to edema, the increase in the mean+/-SE sympathetic firing rate was >2 times larger than in those resistant to edema (36+/-7 versus 15+/-4 bursts per minute, P<0.001) and preceded the development of lung edema. We observed a direct relationship between sympathetic nerve activity and pulmonary artery pressure measured at low and high altitude in the 2 groups (r=0.83, P<0.0001). CONCLUSIONS: With the use of direct measurements of postganglionic sympathetic nerve discharge, these data provide the first evidence for an exaggerated sympathetic activation in subjects prone to high-altitude pulmonary edema both during short-term hypoxic breathing at low altitude and during actual high-altitude exposure. Sympathetic overactivation may contribute to high-altitude pulmonary edema. (+info)
Sympathetic neuronal oscillators are capable of dynamic synchronization.
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In this paper we show that the discharges of sympathetic neurons innervating an identified peripheral target are driven by multiple oscillators that undergo dynamic synchronization when an entraining force, central respiratory drive (CRD), is increased. Activity was recorded from postganglionic sympathetic neurons (PGNs) innervating the caudal ventral artery of the rat tail: (1) at the population level from the ventral collector nerve (VCN); and (2) from pairs of single PGNs recorded simultaneously using a focal recording technique. Autospectral analysis of VCN activity revealed a more prominent rhythmical component in the presence of CRD than in its absence, suggesting that (1) multiple oscillators drive the discharges of PGNs and (2) these oscillators can be entrained and therefore synchronized by CRD. This interpretation was supported by analysis of the firing behavior of PGN pairs. Autocorrelation and cross-correlation analysis showed that pairs were not synchronized in the absence of CRD but showed significant synchronization when CRD was enhanced. Time-evolving spectral analysis and raster plots demonstrated that the temporal stability of PGN-to-PGN and CRD-to-PGN interactions at a given level of CRD were also dynamic in nature, with stable constant phase relationships predominating as CRD was increased. This is the first reported example of dynamic synchronization in populations of single postganglionic sympathetic neurons, and we suggest that, as in sensory processing and motor control, temporal pattern coding may also be an important feature of neuronal discharges in sympathetic pathways. (+info)
Rhythmicity in single fiber postganglionic activity supplying the rat tail.
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Rhythmicity in single fiber postganglionic activity supplying the rat tail. The temporal pattern of ongoing sympathetic vasoconstrictor activity may play an important role for neurovascular transmission. Here we analyzed the activity of postganglionic fibers projecting into the ventral collector nerve of anesthetized and artificially ventilated vagotomized Wistar rats with respect to the presence of rhythmic firing under normocapnic conditions. Most of the fibers studied were likely vasoconstrictor and involved in thermoregulation. Accumulated histograms of sympathetic activity were produced synchronized with the electrocardiogram to detect cardiac rhythmicity, with phrenic nerve activity to detect modulation with the central respiratory cycle, and with tracheal pressure to uncover a reflex modulation associated with artificial ventilation. Sympathetic activity, phrenic activity, and tracheal pressure also were examined by spectral analysis and autocorrelation to detect rhythmicities distinct from respiration. Twenty-seven filaments containing two to seven fibers with spontaneous activity and 51 single fibers were analyzed. Ongoing activity was 1.12 +/- 0.65 imp/s (mean +/- SD, n = 51); conduction velocity was 0.62 +/- 0.06 m/s (n = 30). Cardiac rhythmicity in sympathetic activity was weak (46.2 +/- 16.4%). The dominant rhythm in the activity of 19/27 few-fiber preparations and 37/51 single fibers corresponded to the central respiratory cycle. The pattern consisted of an inhibition during inspiration and an activation in expiration. In 10/19 few-fiber preparations and 21/37 single fibers of this group, there was also a concomitant, less prominent rhythm related to artificial ventilation. By contrast, 8/27 few-fiber preparations and 11/51 single fibers exhibited a dominant pump-related modulation, whereas phrenic-related rhythmicity was subordinate. The dominant rhythm in the activity of two single fibers was related to neither central respiration nor artificial ventilation. We conclude that the ongoing activity of most postganglionic neurons supplying the rat tail is modulated by the central respiratory rhythm generator, suggesting that changes in respiratory drive may alter perfusion of the tail and therefore heat dissipation. Reflex modulation in parallel with artificial ventilation, independent of vagal afferents and possibly due to ventilatory changes of baroreceptor activity, is also an important source of rhythmicity in these neurons. (+info)
Quantitative analysis of the sympathetic innervation of the rat knee joint.
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Retrograde tracing with Fluoro-Gold (FG) was used to identify the complete population of knee joint sympathetic postganglionic efferents in the lumbar sympathetic chain of adult female Wistar rats. In 6 rats, the total number and distribution of FG-labelled neurons in the lumbar sympathetic chain was determined. The rat knee joint is supplied by an average of 187+/-57 sympathetic afferents with the majority at the L3 and L4 levels. Immunohistochemistry using antibodies specific for tyrosine hydroxylase (TH), somatostatin (SS) or vasoactive intestinal polypeptide (VIP) revealed that 33 % of knee joint sympathetic afferents contained TH, 42 % contained VIP, and none contained somatostatin. Retrograde tracing with FG provided accurate and reproducible labelling of the joint-innervating subpopulation of sympathetic efferent neurons. This model lends itself to the further study of the molecular responses of this neuronal population in the various disorders and conditions affecting joints. (+info)
Differential patterns of spinal sympathetic outflow involving a 10-Hz rhythm.
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Time and frequency domain analyses were used to examine the changes in the relationships between the discharges of the inferior cardiac (CN) and vertebral (VN) postganglionic sympathetic nerves produced by electrical activation of the midbrain periaqueductal gray (PAG) in urethan-anesthetized, baroreceptor-denervated cats. CN-VN coherence and phase angle in the 10-Hz band served as measures of the coupling of the central oscillators controlling these nerves. The 10-Hz rhythm in CN and VN discharges was entrained 1:1 to electrical stimuli applied to the PAG at frequencies between 7 and 12 Hz. CN 10-Hz discharges were increased, and VN 10-Hz discharges were decreased when the frequency of PAG stimulation was equal to or above that of the free-running rhythm. In contrast, stimulation of the same PAG sites at lower frequencies increased, albeit disproportionately, the 10-Hz discharges of both nerves. In either case, PAG stimulation significantly increased the phase angle between the two signals (VN 10-Hz activity lagged CN activity); coherence values relating their discharges were little affected. However, the increase in phase angle was significantly more pronounced when the 10-Hz discharges of the two nerves were reciprocally affected. Importantly, partialization of the phase spectrum using the PAG stimuli did not reverse the change in CN-VN phase angle. This observation suggests that the increase in the CN-VN phase angle reflected changes in the phase relations between coupled oscillators in the brain stem rather than the difference in conduction times to the two nerves from the site of PAG stimulation. In contrast to the effects elicited by PAG stimulation, stimulation of the medullary lateral tegmental field induced uniform increases in the 10-Hz discharges of the two nerves and no change in the CN-VN phase angle. Our results demonstrate that changes in the phase relations among coupled brain stem 10-Hz oscillators are accompanied by differential patterns of spinal sympathetic outflow. The reciprocal changes in CN and VN discharges produced by PAG stimulation are consistent with the pattern of spinal sympathetic outflow expected during the defense reaction. (+info)
High thoracic epidural anesthesia does not inhibit sympathetic nerve activity in the lower extremities.
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BACKGROUND: Sympathetic nerve activity was recorded in the leg during high thoracic epidural anesthesia with a segmental sensory blockade of the upper thoracic dermatomes to test the hypothesis that the sympathetic blockade accompanying thoracic epidural anesthesia includes caudal parts of the sympathetic nervous system. METHODS: Experiments were performed on 10 patients scheduled for thoracotomy. An epidural catheter was inserted at the T3-T4 or T4-T5 interspace. In the main protocol (seven patients), blood pressure, heart rate, and skin temperature (big toe, thumb) were continuously monitored, and multiunit postganglionic sympathetic nerve activity was recorded with a tungsten microelectrode in a muscle-innervating fascicle of the peroneal nerve. After baseline data collection, muscle sympathetic nerve activity was recorded for an additional 45-min period after epidural injection of 4-6 ml bupivacaine, 5 mg/ml. In an additional three patients, the effects of thoracic epidural anesthesia on skin-innervating sympathetic nerve activity were qualitatively assessed. RESULTS: Activation of thoracic epidural anesthesia caused no significant changes in peroneal muscle sympathetic nerve activity (n = 7), blood pressure, or heart rate. Skin temperature increased significantly in the hand 15 min after activation of the blockade, from 32.7 +/- 2.4 degrees C to 34.4 +/- 1.5 degrees C (mean +/- SD), whereas no changes were observed in foot temperature. The sensory blockade extended from T1 (C4-T2) to T8 (T6-T11). CONCLUSIONS: A high thoracic epidural anesthesia with adequate sensory blockade of upper thoracic dermatomes may be achieved without blockade of caudal parts of the sympathetic nervous system. This finding differs from that of earlier studies that used indirect methods to evaluate changes in sympathetic nerve activity. (+info)
Coherent rhythmic discharges in sympathetic nerves supplying thermoregulatory circulations in the rat.
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1. In anaesthetised rats, activity recorded from sympathetic postganglionic neurones innervating the tail circulation has characteristic rhythmicity (0.4-1.2 Hz). At the population level this rhythmicity can be seen as a peak (T-peak) in autospectra of sympathetic activity recorded from ventral collector nerves (VCNs). 2. Here we investigated whether nerves supplying thermoregulatory circulations share common rhythmic discharges at T-peak frequency. Activity was recorded from nerve pairs consisting of left ventral collector nerve (LVCN) and one of the following: right ventral collector nerve (RVCN), left dorsal collector nerve (DCN), left saphenous nerve (SN) or left renal nerve (RN). 3. During central apnoea, T-peak frequencies in RVCN autospectra were similar to those of simultaneously recorded LVCN and these activities were coherent. Similar observations were made for nerve pairs involving LVCN-DCN and LVCN-SN. In contrast, autospectra of RN activity did not contain T-peaks. 4. In comparison to the peaks in autospectra of RN activity, when the frequency of rhythmic phrenic nerve activity was manipulated T-peaks in VCN, DCN and SN autospectra did not show obligatory 1:1 locking. 5. We conclude that T-peaks are a robust feature of autospectra of sympathetic discharges supplying thermoregulatory circulation but not those influencing the kidney. The high coherence demonstrated between the T-peak discharges is consistent with the view that common/coupled oscillators located within the CNS influence cutaneous vasoconstrictor sympathetic activity. (+info)