Thoracic White Rami Research Articles

Are pre-ganglionic neurones recruited in a set order?

The idea that, like somatic motor neurones, sympathetic pre-ganglionic neurones are engaged to fire in a pre-determined recruitment order, was investigated in chloralose-anaesthetized cats. Ongoing pre-ganglionic spike activity was recorded from fine filaments of otherwise intact thoracic white rami, while post-ganglionic activity was recorded from the whole inferior cardiac nerve (ICN). Spikes of individual pre-ganglionic fibres were extracted from few-fibre recordings by spike shape analysis. Presumed cardiac pre-ganglionic fibres were further selected by the spike-triggered average of ICN activity, which showed a clear peak when triggered by their spikes. To test whether particular pre-ganglionic neurones were recruited to fire in a set time sequence, the spontaneous spike trains of fibres in the same white ramus were compared by cross correlation. In all 24 cases the cross correlograms showed a central peak (width 163 +/- 15 ms), indicating that the two neurones tended to fire together. In 23 of the 24 cases that peak spanned the zero point on the time axis, showing that each neurone could fire either first or second. To test whether pre-ganglionic neurones were recruited in a set order with respect to burst amplitude, the firing of individual pre-ganglionic neurones was compared with the strength of the corresponding post-ganglionic burst discharge, on a heartbeat-by-heartbeat basis. Pre-ganglionic neurone firing was probabilistic: each neurone fired with only a minority of post-ganglionic bursts. Firing probability increased linearly with burst amplitude (30 of 30 cases). The slope of the relation varied between units, but its intercept was always close to the origin (zero pre-ganglionic firing probability at zero post-ganglionic burst size). The data indicate that, at least under these conditions, sympathetic pre-ganglionic neurones follow no set recruitment sequence in either their firing times or with respect to the strength of the autonomic motor output.

Spinal segments communicating resting sympathetic activity to postganglionic nerves of the stellate ganglion.

It has been shown earlier using sympathetic reflexes and anatomic techniques that preganglionic neurons controlling different effectors occupy wide and overlapping ranges of adjacent segments in the spinal cord (cardiac: T1-T7, vertebral: T2-T8). Because, however, the majority of preganglionic neurons are silent at resting states, the present study was designed to estimate the segmental map of subsets of these neurons including only those active at rest using simultaneous recordings from the inferior cardiac and vertebral nerves, under chloralose-urethan or urethan anesthesia. In 22 cats, thoracic white rami T1-T8 were cut in a sequential manner. Three-minute-long data segments were recorded between sectionings and analyzed in the frequency domain using the fast Fourier transform. We found that cardiac and vertebral active maps involved segments T3-T5 and T4-T8, respectively. In individual experiments, however, most of the power of rhythmic activity originated from only one or two segments and the dominant segments for the two nerves never overlapped. Moreover, the separation between dominant segments generating cardiac and vertebral nerve discharges was wider and the distribution of tonically active preganglionic neurons projecting to each nerve was narrower under urethan than chloralose-urethan anesthesia. We conclude that the proportion of active to quiescent preganglionic neurons regulating cardiac and vertebral nerve discharges varies from spinal segment to segment and that active neurons projecting to these nerves are nonoverlapping.

Topographic relationship of neurotensin-containing axon terminals with cardiac and noncardiac principal ganglion cells in the stellate ganglia of the cat

The pattern of association between neurotensin (NT)-immunoreactive (NTIR) preganglionic nerve terminals and cardiac and noncardiac neurons in the stellate ganglion of the cat is analyzed, based on the finding of an excitatory modulation effect of exogenous NT on cardiac functions. For this purpose, NT-containing terminals were labeled by immunohistochemistry, and ganglion cells were detected by retrograde labeling of cardiac and vertebral nerves to identify cardiac and noncardiac neurons. To determine a possible regional localization of NTIR terminals and ganglion cells, the ganglia were divided into four areas: caudal, dorsomedial, cranial, and ventromedial, related to the two major afferent nerves (thoracic white rami 3 [T3WR] and 2 [T2WR]) and the two efferent nerves (vertebral and cardiac). NTIR terminals were widespread in the complete ganglion tissue; they covered practically all the regions explored, although two clusters of high concentration of NTIR terminals were detected in the cranial and caudal areas. By retrograde labelling it was found that cardiac cells were arranged around the exit of the cardiac nerve and that the vertebral neurons were extended from the exit of the vertebral nerve to the entrance of T3WR. The finding of association of NTIR terminals with cardiac neurons may account for the cardioregulatory effect of NT; however, since the presence of NTIR terminals close to the noncardiac neurons is notorious, other regulatory functions of NT must be considered.

Topographic relationship of neurotensin‐containing axon terminals with cardiac and noncardiac principal ganglion cells in the stellate ganglia of the cat

The pattern of association between neurotensin (NT)-immunoreactive (NTIR) preganglionic nerve terminals and cardiac and noncardiac neurons in the stellate ganglion of the cat is analyzed, based on the finding of an excitatory modulation effect of exogenous NT on cardiac functions. For this purpose, NT-containing terminals were labeled by immunohistochemistry, and ganglion cells were detected by retrograde labeling of cardiac and vertebral nerves to identify cardiac and noncardiac neurons. To determine a possible regional localization of NTIR terminals and ganglion cells, the ganglia were divided into four areas: caudal, dorsomedial, cranial, and ventromedial, related to the two major afferent nerves (thoracic white rami 3 [T3WR] and 2 [T2WR]) and the two efferent nerves (vertebral and cardiac). NTIR terminals were widespread in the complete ganglion tissue; they covered practically all the regions explored, although two clusters of high concentration of NTIR terminals were detected in the cranial and caudal areas. By retrograde labeling it was found that cardiac cells were arranged around the exit of the cardiac nerve and that the vertebral neurons were extended from the exit of the vertebral nerve to the entrance of T3WR. The finding of association of NTIR terminals with cardiac neurons may account for the cardioregulatory effect of NT; however, since the presence of NTIR terminals close to the noncardiac neurons is notorious, other regulatory functions of NT must be considered. Synapse 25:277–284, 1997. © 1997 Wiley-Liss, Inc.

Different effects of respiratory and metabolic acidosis on preganglionic sympathetic nerve activity

We studied sympathetic nerve activity (SNA) responses, recorded in multifiber preparations of left third thoracic white ramus, to respiratory or isocapnic metabolic acidosis or to CO2 enhancement at constant pH in chloralose-anesthetized paralyzed artificially ventilated cats. Cardiopulmonary, baro-, and peripheral chemoreceptors were denervated by bilaterally cutting vagus and carotid sinus nerves. Acidosis was induced by either decreasing artificial ventilation or infusing HCl (0.5 M i.v.). Both respiratory and isocapnic metabolic acidosis induced a decrease in local extracellular pH, measured directly with pH-sensitive microelectrodes within medulla region containing sympathoexcitatory bulbospinal neurons. The magnitude of changes in medullary pH was independent of the way systemic acidosis was generated. Despite uniformity of changes in local medullary extracellular pH due to systemic respiratory or isocapnic metabolic acidosis, different responses were observed in preganglionic SNA. Isocapnic metabolic acidosis resulted in a slight increase in SNA, averaging 6.4% per 0.05 systemic pH unit decrease. In contrast, respiratory acidosis induced by decreasing artificial ventilation produced a more pronounced increase of SNA, reaching peak changes of approximately 70% compared with control level with normal blood gases, an average increase of 13% per 0.05 systemic pH unit decrease. We conclude that systemic CO2 and H+ concentrations represent different stimuli to sympathetic nervous system. Despite similar changes of local extracellular pH within rostral ventrolateral medulla during systemic acidosis, different responses of SNA suggest other sites or as yet unknown additional effects of CO2 as being responsible for excitation of sympathetic activity.

Preganglionic axons from the third thoracic spinal segment fail to induce long-term potentiation in the superior cervical ganglion of the cat.

A stimulus train to preganglionic axons produces long-term potentiation (LTP) of population responses of sympathetic ganglion cells evoked by the same or by other converging axons. The present study shows that preganglionic axons emerging from the spinal cord in different thoracic rami, and converging onto a common pool of ganglion cells that innervate a single target, differ in their ability to induce LTP. In anesthetized cats under partial nicotinic block with hexamethonium, the nictitating-membrane (NM) contraction evoked by stimulation of the first (T1) and third (T3) thoracic white rami (WR) was recorded. Each ramus produced a contraction of similar amplitude. In contrast, the homosynaptic potentiation produced by a 40-Hz 10-s train differed markedly. T1WR produced a potentiation of duration comparable to that produced by stimulation of the cervical sympathetic trunk, while T3WR produced either no potentiation or a potentiation of much shorter duration. The NM response evoked by T3WR, however, was potentiated by similar extent and duration as was the response evoked by T1WR when the train was applied to T1WR (heterosynaptic LTP). This suggests that the ganglionic synapses made by T3WR possess the mechanism for expressing LTP. Conversely, T3WR was ineffective at potentiating heterosynaptically the NM response evoked by T1WR. These results suggest that the ability to produce or release the LTP inducer varies markedly among sympathetic preganglionic neurons.

Long-term potentiation of nicotinic transmission by a heterosynaptic mechanism in the stellate ganglion of the cat.

1. In the anesthetized, scopolamine-treated cat, the compound action potential (CAP) evoked by a single supramaximal shock to the third thoracic white ramus (T3WR) was recorded in the inferior cardiac nerve (ICN). The CAP was depressed in a dose-dependent manner by the intravenous administration of the nicotinic antagonist hexamethonium (C6). 2. During steady intravenous infusion of C6, which reduced the amplitude of the CAP by 80-90%, a short train of stimuli (few seconds, 10-40 Hz) to the sympathetic trunk just below T4WR potentiated the CAP for periods of tens of minutes to 1-2 h (heterosynaptic long-term potentiation, LTP). An LTP of similar time course was obtained when both train and single shock were applied to T3WR (homosynaptic LTP). Magnitude and duration of the heterosynaptic LTP were dependent on number, frequency, and intensity of the stimuli. No LTP was produced by a train to the ICN. Heterosynaptic LTP was also observed in the absence of C6. Because of the limited subliminal fringe of the test input under this condition, the LTP was of small magnitude. Heterosynaptic LTP also of the heart rate (HR) response to a test stimulus was observed after a conditioning train. 3. The conditioning train produced a displacement to the right of the dose-response curve for C6. The intravenous dose of C6 required for 50% attenuation of the test CAP increased from 0.84 +/- 0.15 (SE) mg/kg pretrain to 2.56 +/- 0.46 mg/kg posttrain (n = 5, P less than 0.01).(ABSTRACT TRUNCATED AT 250 WORDS)

Spinal segmental sympathetic outflow to cervical sympathetic trunk, vertebral nerve, inferior cardiac nerve and sympathetic fibres in the thoracic vagus

The spinal segmental localization of preganglionic neurons which convey activity to the sympathetic nerves, i.e. vertebral nerve, right inferior cardiac nerve, sympathetic fibres in the thoracic vagus and cervical sympathetic trunk, was determined on the right side in chloralose anaesthetized cats. For that purpose the upper thoracic white rami were electrically stimulated with a single pulse, suprathreshold for B and C fibres, and the evoked responses were recorded in the sympathetic nerves. The relative preganglionic input from each segment of the spinal cord to the four sympathetic nerves was determined from the size of the evoked responses. It was found that each sympathetic nerve receives a maximum preganglionic input from one segment of the spinal cord (dominant segment) and that the preganglionic input gradually decreased from neighbouring segments. The spinal segmental preganglionic outflow to the cervical sympathetic trunk, thoracic vagus, right inferior cardiac nerve and vertebral nerve gradually shifted from the most rostral to the most caudal spinal cord segments. In some cases, a marked postganglionic component was found in the cervical sympathetic trunk. It was evoked by preganglionic input from the same spinal cord segments which transmitted activity to the vertebral nerve. These results indicate that there is a fixed relation between the spinal segmental localization of preganglionic neurons and the branch of the stellate ganglion receiving the input from these neurons.

Selective control of sympathetic pathways to the kidney, spleen and intestine by the ventrolateral medulla in rats.

1. Electrical activity of multifibre renal, splenic, mesenteric and greater splanchnic nerves and 13th thoracic white rami was recorded in artificially respired, urethane-anaesthetized rats. Discharge of neurones in the rostral ventrolateral medulla was blocked by unilateral microinjections of the inhibitory amino acid glycine and effects on the electrical activity of these sympathetic nerves were compared. 2. Blockade of the rostral ventrolateral medulla caused greater decreases in discharge of renal than splenic nerves and had no consistent effect on mesenteric nerves. This blockade also decreased the discharge of the preganglionic white rami more than that of the preganglionic splanchnic nerves. 3. Postganglionic responses to rostral ventrolateral medulla blockade were always greater than preganglionic responses. 4. The arterial pressure and renal nerve responses to rostral ventrolateral medulla blockade in urethane-anaesthetized rats were not different from those in rats anaesthetized with alpha-chloralose. 5. These findings demonstrate that pre- and postganglionic sympathetic pathways to the kidney are more dependent upon excitatory drive from the rostral ventrolateral medulla than pathways directed to the spleen and intestine.

Control of the heart rate by sympathetic nerves in cats

Pre- and postganglionic sympathetic nerves were electrically stimulated and heart rate was recorded in chloralose-anaesthetised cats. The vagal nerves and white rami were cut on both sides. Electrical stimulation was performed with a 15- or 30-s train of 0.2-ms pulses at a frequency of 30 Hz. The control heart rate was 150 beats/min. Heart rate was increased when the T 3 white ramus on the left (52 beats/min above control) and T 3, T 4 white rami on the right side (100 beats/min above control) were stimulated electrically. The magnitude of the heart rate increase declined when the neighbouring thoracic white rami were stimulated. The increase of the heart rate was caused by group B preganglionic fibres. Electrical stimulation of the sympathetic fibres in the right vagus nerve and the right inferior cardiac nerve increased the heart rate by 92 beats/min and by 67 beats/min above the control level respectively. Electrical stimulation of the left inferior cardiac nerve, the left middle cardiac nerve and the sympathetic fibres in the left vagus nerve resulted in an increase of the heart rate of 43 beats/min, 30 beats/min and 49 beats/min from the control level respectively. This indicates that a majority of the preganglionic cardiac sympathetic fibres, whose activity influences the heart rate, originate from the T 3 and T 4 segments of the spinal cord. The majority of the postganglionic cardiac sympathetic fibres which affect the heart rate are located in the vagal nerves.

Spinal interneurons with sympathetic nerve-related activity.

This study tested the hypothesis that at least some brain stem and reflex control of sympathetic outflow is mediated over pathways containing spinal interneurons. The vicinity of the intermediolateral nucleus (IML) of the third thoracic spinal segment was searched for neurons with spontaneous activity correlated to that in the inferior cardiac post-ganglionic sympathetic nerve of 16 baroreceptor-denervated cats anesthetized with Dial-urethane. Section of the carotid sinus, aortic depressor, and vagus nerves prevented the coupling of sympathetic and nonsympathetic networks by pulse synchronous baroreceptor activity. Spike-triggered averaging revealed the existence of two types of spinal neurons with sympathetic nerve-related activity. Preganglionic sympathetic neurons (PSN; n = 33) were antidromically activated by electrical stimulation of their axons in the third thoracic white ramus. Four observations suggest that the second group of neurons with sympathetic nerve-related activity (n = 18) were spinal interneurons (SIN) in pathways that excite PSN. First, these neurons could not be antidromically activated by stimulation of the segmental white ramus. Second, the intervals between spontaneous unit spike occurrence and inferior cardiac nerve activity were similar for SIN and PSN. Third, SIN and PSN were activated with nearly identical onset latencies by electrical stimulation of medullary sympathoexcitatory sites. Fourth, SIN were excited by intensities of cardiac sympathetic afferent stimulation that also activated PSN and the inferior cardiac nerve. SIN and PSN were distinguished on the basis of their spontaneous firing patterns; i.e., interspike intervals of SIN were significantly shorter than those of PSN.(ABSTRACT TRUNCATED AT 250 WORDS)

Possible projections from regions of paraventricular and supraoptic nuclei to the spinal cord: electrophysiological studies

The existence of monosynaptic connections between neurons in the paraeventricular nucleus (PVN) of the hypothalamus and the intermediolateral cell column (ILC) of the spinal cord was studied by electrophysiological techniques in chloralose-anesthetized cats. Sympathetic peganglionic discharges (recorded from the 2nd or 3rd thoracic white ramus) were evoked by microstimulation of certain regions in or near the PVN with short train of pulses and below 50μA current. By recording responces of ‘identified’ and ‘non-identified’ neurosecretory cells in the PVN and supraoptic nucleus (SON) to stimulation of the ILC of the thoracic cord, it was possible to identify antidromically evoked action potentials in 9 out of 297 neurons tested. Among them, 2 neurons were also antidromically excited by the pituitary stalk stimulation, 5 were orthodromically excited by the same stimulus and the remaining 2 were not excited by the stalk stimulation. Our results indicate that some PVN neurons, though small in number, send axons directly to the ILC of the cord, and that a very few neurons among these also send their axons to the pituitary gland.

Intracellular recordings from sympathetic preganglionic neurones

In anaesthetised cats the response of the soma dendritic region of sympathetic preganglionic neurones (SPN) recorded intracellularly in T 3 spinal segment was studied following excitation of third thoracic white ramus and following orthodromic inputs. Most cells had action potentials of short duration. Many cells were active. Decreases in membrane potential were relatively short lasting, < 40 msec and a change of 5 mV was sufficient to discharge the cell. Increases in membrane potential were also evident.

Ultrastructural identification of afferent fibers of cardiac origin in thoracic sympathetic nerves in the dog.

While cardiac afferent nerve activity has been recorded from the ventrolateral (VLCN) and ventromedial (VMCN) cardiac nerves, left dorsal and ventral ansae subclaviae, and left upper thoracic white rami communicantes, little anatomical evidence for the existence of afferent fibers in these nerves has been reported. This study was designed to characterize the normal ultrastructure of the above nerves and to identify afferent fibers in them through Wallerian degeneration produced by dorsal root ganglionectomy. Laminectomies followed by dorsal root ganglionectomies were performed on left thoracic roots T1-T4 in six mongrel dogs. The nerves to be examined were removed from two animals at 1, 2, and 3 weeks following ganglionectomy and prepared for electron microscopy. Control nerves were obtained from two normal dogs. Degenerating nonmyelinated fibers were characterized by watery axoplasm containing clumps of electron-dense material. Degenerating myelinated fibers were distinguished by the separation of their myelin lamellae, producing characteristic whorls. After three weeks, afferent nonmyelinated axons had degenerated in all nerves, leaving only layered processes of Schwann cells in these areas. Approximately 5-15% of the fibers in each nerve degenerated, indicating their afferent nature. Of these fibers, 85-90% were nonmyelinated C fibers and the remainder myelinated Adelta fibers. These results indicate participation of both Adelta fibers and a large population of C fibers in transmission of cardiac afferent activity.

Categories of axons in the inferior cardiac nerve of the cat.

Myelinated and unmyelinated axons in the inferior cardiac nerve of the cat were examined to determine how many axons were (1) sensory, (2) preganglionic sympathetic, and (3) postganglionic sympathetic. In one group of cats, a segment was removed from the middle of the inferior cardiac nerve as a control, and the proximal and distal stumps of the nerve were examined one week later. In another group of cats, the control segment of nerve was removed and the first thoracic white ramus communicans and sympathetic trunk were cut proximal to the stellate ganglion, followed in one week by examination of the proximal and distal stumps of the inferior cardiac nerve. In still another group of cats, the first five thoracic spinal nerves were cut just distal to the dorsal root ganglion. The counts of myelinated and unmyelinated axons after these surgical procedures indicated that, in the cat inferior cardiac nerve, all or almost all of the approximately 30,000 unmyelinated axons and 10 percent of the myelinated axons are postganglionic sympathetic fibers, and that approximately 90 percent of the myelinated axons are sensory.

Response of left ventricular mechanoreceptors to changes in pressure and muscle length.

SummaryWe conclude that the increase in isovolumetrically developed intraventric-ular pressure is associated with an enhanced activity of cardiac sympathetic afferents traversing the left upper thoracic white rami communicantes, as reported by Hess et al. (8). Moreover, the sympathetic afferent nerve fibers respond to alteration in myocardial muscle length occurring in isobaric diastole and thus respond to a displacement stimulus as well as to a pressure stimulus.

Sympathetic afferent nerve activity of right heart origin.

Six mongrel dogs anesthetized with sodium pentobarbital and paralyzed with gallamine triethiodide were studied on total cardiopulmonary bypass. This study verified the existence of right heart mechanoreceptors whose afferent nerves traverse the upper thoracic white rami communicantes. these mechanoreceptors were studied by observing changes in average maximum, and total nerve spike frequency when right atrial and right ventricular systolic and diastolic pressures were altered by means of intracardiac balloons. Receptors that responded to volume and pressure changes were found in both the right atrium and right ventricle. Nerve activity in these afferents increased with increasing right atrial and right ventricular pressures. These mechanoreceptors were more responsive in the upper physiological ranges of right heart pressures. In most nerve fibers studied, maximum activity occurred during both right atrial and right ventricular diastole.

Pulmonary afferent activity recorded from sympathetic nerves.

This study in mongrel dogs, anesthetized with sodium pentobarbital, verified the existence of pulmonary receptors whose afferents traverse the right and left upper thoracic white rami communicantes. These receptors responded to lung inflation as well as pinching of the lung parenchyma and were nonadapting in nature. In some fibers, increases in afferent activity were also observed when the pulmonary artery and veins were mechanically stimulated by probing. Conduction velocities of these afferents were measured in single-fiber preparations and were of the Adelta fiber type.

The spinal route of sympatho-inhibitory pathways descending from the medulla oblongata.

1. The effect of making discrete lesions in the cervical spinal cord on the brainstem elicited inhibition of a spinal somato-sympathetic reflex response has been studied in anaesthetized cats. 2. Electrical stimulation within three areas of the medulla caused an inhibition of the spinal component of the reflex response elicited in thoracic white rami communicantes by stimulation of intercostal nerves. The three medullary areas studied were the ventrolateral medulla and the caudal rephe nucleus, from where bulbospinal monoamine neurones originate, and the ventromedial reticular formation. 3. The inhibitory effects of stimulation in the ventrolateral medulla and raphe nucleus were abolished by the destruction of parts of the ipsilateral dorsolateral funiculus of the cervical spinal cord, whereas the inhibition produced by ventromedial reticular formation stimulation was abolished by lesions which included part of the ventral quadrant of the cord. 4. The time course of the inhibitory effects of electrical stimulation of descending sympatho-inhibitory tracts in the cervical spinal cord was studied in unanaesthetized decerebrate cats spinalized at C1. Inhibition obtained from the dorsolateral funiculus characteristically had a longer time to onset than inhibition obtained from the ventrolateral and ventral funiculi.

The influence of bulbospinal monoaminergic pathways on sympathetic nerve activity.

1. Spontaneous and reflex activity was recorded from renal and splanchnic nerves and thoracic white rami during discrete electrical stimulation within the medulla oblongata of anaesthetized cats.2. Inhibition or excitation of spontaneous sympathetic nerve activity was obtained from several medullary regions.3. The long-circuited reflex elicited in renal nerves and the spinally mediated reflex discharge produced in white rami by single shock stimulation of intercostal nerves were inhibited by stimulation within the sympatho-inhibitory areas of the medulla.4. Activation of spontaneous sympathetic nerve activity or inhibition of spontaneous and reflex sympathetic nerve activity was obtained during electrical stimulation within the lateral funiculi of the cervical spinal cord in unanaesthetized decerebrate cats, spinalized at C1.5. There was a correlation between the position of some sympatho-inhibitory regions of the medulla and spinal cord and the position of the cell bodies and axons of descending monoamine-containing neurones.6. Intravenous administration of the precursor of noradrenaline, L-DOPA, to unanaesthetized decerebrate cats, spinalized at C1, was followed by a depression of spontaneous activity in renal nerves and reflex responses elicited in renal nerves and white rami.7. Similarly the precursor of 5-hydroxytryptamine, 5-HTP, caused a depression of reflex activity elicited in renal nerves and white rami, but had no effect on spontaneous renal nerve activity.8. It is suggested that there exist both noradrenergic and tryptaminergic pathways which descend to the spinal cord from the medulla and which are inhibitory to sympathetic outflow.