CLIN. AND EXPER. HYPERTENSION, 17(1&2), 345-359 (1995)

PROPERTIES OF PREGANGLIONIC AND POSTGANGLIONIC NEURONES IN VASOCONSTRICTOR PATHWAYS OF RATS AND

GUINEA PIGS.

Elspeth M. McLachlan Prince of Wales Medical Research Institute

Randwick, NSW 2031, Australia.

Keywords: preganglionic postganglionic excitatory potentials inhibitory potentials tonic activity

ABSTRACT

The electrophysiological properties of pre- and postganglionic neurones and their synaptic inputs have been examined in both in vivo and in vitro preparations. Electrically, both neurone types have similar low resting conductance and compact dendritic trees. In preganglionic vasoconstrictor neurones, both slow and fast excitatory and fast inhibitory potentials are probably involved in baroreceptor reflexes, discharge being initiated after summation. In contrast, postganglionic vasoconstrictor neurones receive only one type of fast excitatory input. One of the converging preganglionic inputs has a very high safety factor and always fires the postganglionic neurone ensuring that the centrally- derived pattern of discharge reaches the neurovascular junctions. We do not know if the other subthreshold inputs summate during natural activity in vivo, as it is not known whether functionally distinct preganglionic inputs converge on vasoconstrictor neurones in ganglia.

345

Copyright @ 1995 by Marcel Dekker, Inc.

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INTRODUCTION A large proportion of the sympathetic nervous system is concerned

with distributing the electrical signals which initiate and maintain the degree of constriction of blood vessels throughout the body. The pattern of this activity arises within the central nervous system, being determined by the summed effects of supraspinal and spinal synaptic connections which impinge on the final output unit, the preganglionic vasoconstrictor neurone. Preganglionic signals are distributed by divergence of their terminals within sympathetic ganglia to influence many postganglionic neurones which then project to the peripheral vasculature. This nervous discharge determines the level of the arterial blood pressure during short term physiological adjustments, as well as when more extreme demands are placed on the circulation, and is responsible for the redistribution of blood to different tissues during specific activities. The patterns of neuronal discharge are superimposed on an overall level of "vasoconstrictor tone" regulated by baroreceptor and chemoreceptor reflexes which normally maintain adequate cerebral and coronary perfusion. Vasoconstrictor neurones can be identified in single unit recordings by the presence of a marked rhythm in the discharge equivalent to that of the cardiac cycle (1, 2). This functional marker can be recognized both in preganglionic and postganglionic axons.

ANATOMICAL ARRANGEMENT The anatomical distribution in the spinal cord and peripheral ganglia

of neurones which participate in vasomotor control has been well described. Tracing studies in animals (3, 4) indicate that preganglionic vasoconstrictor neurones are concentrated in the lateral parts of the thoracolumbar intermediolateral column extending into the lateral funiculi; this lateral location is the site of physiological recordings from units with baroreceptor-linked activity ( 5 ) . These neurones have some of the smallest somata of all the preganglionic population (4) and

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SYNAPTIC POTENTIALS IN VASOCONSTRICTOR PATHWAYS 347

preganglionic muscle vasoconstrictor neurones projecting in peripheral nerves have generally low conduction velocities (6).

The thinly myelinated or unmyelinated preganglionic axons pass around the ventral horn and exit the spinal column via the ventral roots and white rami. The preganglionic axons either branch into several segmental ganglia of the paravertebral chain (7) or they cross the chain via one of the splanchnic nerves to the prevertebral ganglia; within the ganglia they branch further to contact a number of postganglionic neurones. It is clear on anatomical grounds that the divergence of preganglionic neurones potentially yields an amplification of the vasoconstrictor signal - the numerical ratio of post- to preganglionic neurones is 10 to 100:1, increasing with species size.

Paravertebral neurones project to the somatic vasculature of the cranium, trunk and limbs (8) and to the blood vessels of thoracic (9) and pelvic viscera (10). Vasoconstrictor neurones supplying the vessels of the abdominal viscera lie mainly in prevertebral ganglia amongst neurones with other actions in the visceral organs (11). The kidney has associated renal ganglia (12, 13). Thus the vasoconstrictor pathways from the spinal outflow to the vasculature are clearly organized according to their target organ. Vasoconstrictor neurones tend to be smaller than postganglionic neurones with other targets (14, 15).

DISCHARGE PATTERNS IN VIVO From studies of the patterns of activity in nerves to different targets,

it is evident that muscle and visceral vasoconstrictor neurones have a predominant role in the control of peripheral resistance, whereas the activity of most cutaneous vasoconstrictor neurones (particularly in man) are regulated primarily for thermoregulation (1). Vasoconstrictor activity in muscle nerves in v i m consists of short sequences of pulse- synchronous bursts (indicating the discharge of a number of coincident units) with periods of silence. The overall frequency of bursts is extremely variable between, but not within, individuals being less than the cardiac frequency except when the arterial pressure is low (16). In

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single postganglionic neurones, ongoing vasoconstrictor discharge has a mean resting frequency of only about 1-2 Hz in anaesthetized cats and rats(1) and in conscious humans (17). This is a much lower frequency than the cardiac rhythm but post R-wave histograms reveal the characteristic pulse-linked inhibition arising from baroreceptors. It is perhaps surprising that the discharge frequency of the neural output signal for vasoconstriction in different species seems to be so similar.

Hz in anaesthetized animals (2), or slightly higher when recorded intracellularly (18, 19), possibly because of surgical stress. Action potentials in these neurones arise after the integration of excitatory and inhibitory synaptic inputs (see Fig. 1). It has been possible to examine changes in synaptic activity during baroreceptor reflexes (19). When pressure in an isolated carotid sinus was manipulated so as to activate arterial baroreceptors, discharge frequency decreased and vice versa . Direct pulsations superimposed on a mean perfusion pressure of 100 mm Hg applied to the carotid sinus evoked a barrage of fast inhibitory synaptic potentials (fi.s.ps) and a decreased action potential discharge. Discrete fast excitatory synaptic potentials (fe.s.ps) could not be distinguished during the depolarization which led to the increased discharge when the baroreceptors were inactivated; rather, the membrane depolarization was relatively smooth. These patterns of synaptic activity in baroreflex pathways can now be explained on the basis of the in vitro analyses discussed below. In contrast, inspiration- related ramps of fe.s.ps resembling those in respiratory motoneurones have been described in preganglionic neurones (20).

Intracellular recordings from sympathetic postganglionic neurones (22, 23) differ from those in central neurones in that there are no detectable fi.s.ps. Subthreshold fe.s.ps and action potentials can be distinguished, with discharge frequencies of 1-2 Hz in a range of anaesthetized animals (21), ongoing activity being less typical of neurones with non-vascular targets (22). Action potentials can arise directly from the baseline with little or no afterhyperpolarization;

Preganglionic neurones also discharge at average frequencies of 1-2

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SYNAPTIC POTENTIALS IN VASOCONSTRICTOR PATHWAYS 349

Preganglionic neurone - integration of many small excitatory and inhibitory inputs

1 s Post-ganglionic neurone - only a few excitatory inputs

summation of weak Inputs

1 s

FIG 1. Intracellular recordings of membrane potential in sympathetic neurones in vivo. Records from preganglionic neurone in T3 spinal cord of cat anaesthetized with pentobarbitone (modified from data in (21)) and from postganglionic neurone in superior cervical ganglion of rabbit anaesthetized with chloralose-urethane (modified from data in

(25)).

others arise from a small preceding depolarization resulting from summation of a sequence of fe.s.ps (see Fig. 1; (23)). Overall, frequency increases and bursting occurs in larger species with more summation of subthreshold fe.s.ps; short interspike intervals can occur in human postganglionic vasoconstrictor axons (17). Again in vitro analyses have clarified the differences between preganglionic inputs (see below).

PROPERTIES OF SYMPATHETIC NEURONES IN VZTRO. The mechanisms underlying these events are difficult to identify in

vivo when the neurones are affected by synaptic activity in multiple unknown inputs as well as being hard to impale. However, isolated preparations of sympathetic ganglia with intact connections and of

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350 McLACHLAN

slices of thoracic spinal cord have been studied. By using graded voltage of electrical stimulation to elicit synaptic responses, the characteristics of different inputs have been analysed.

PrePanPlionic Neurones Preganglionic neurones in the upper thoracic spinal cord have been

impaled in slices maintained in vitro.. Their electrophysiological properties are similar when recorded with an intracellular electrode in transverse slices from adult animals (24, 25) and somewhat different in neurones of neonatal rats (26, 27) which show spontaneous activity and evidence of electrical coupling.

We have used conventional high resistance microelectrodes to record from preganglionic neurones in horizontal slices of the upper thoracic spinal cord of rats (at 22-28 days of age when most of the descending pathways have developed). The action potentials resemble those in cat sympathetic preganglionic neurones (24)] and rat and guinea pig vagal neurones (28-30). Passive membrane properties (see Table) and morphology with 3-7 fine branching dendrites (after filling with biocytin) also resemble those of vagal neurones (30). All neurones had low resting conductances and the time course of electrotonic potentials recorded at the soma did not deviate significantly from single exponentials. This indicates that the dendritic trees are electrically short so that a somatic microelectrode can provide adequate voltage clamp control during analysis except of high frequency conductance changes. Using this technique, we have described the two calcium-dependent potassium currents underlying the long afterhyperpolarization. These currents have characteristics identical to those recorded in vagal neurones (28, 30) and in some sympathetic postganglionic neurones (31, 32).

Most preganglionic neurones in slices have ongoing spontaneous fi.s.ps at frequencies which interfere with measurements of membrane characteristics. These fi.s.ps have recently been shown to be due to glycine release from local neuronal circuits (27); they involve a brief

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SYNAPTIC POTENTIALS IN VASOCONSTRICTOR PATHWAYS 35 1

TABLE

Pre (n=15) Post (n=29) Resting membrane potential (mV) -57 k 2 -54 k 2

(-41 - -72) (-40 - -68) Input resistance (MQ) 254 k 31 138 k 12

Time constant (ms) 26f4 17+ 1 (77 - 555) (30 - 286)

(9 - 57) (7-32) Input capacitance (pF) 109 k 11 131 k 10

(62 - 217) (62 - 253)

Values are means f standard error of mean with the range of values presented in parentheses below. Data from preganglionic neurones in Tl-T3 spinal cord slices ( P. Sah) and postganglionic neurones in isolated stellate ganglia (experiments with L. Melnichenko).

increase in chloride conductance. Bicuculline-sensitive fi.s.ps of similar time course are elicited in some neurones by stimulation in the lateral funiculi [Inokuchi, 1992b #lo331 implying that other inputs are GABAergic. It is not clear which of these inputs is responsible for the fi.s.ps observed during baroreceptor reflexes, i.e whether or not there are inhibitory pathways of supraspinal origin.

preparations, fe.s.ps elicited in preganglionic neurones by stimulation of descending axons in the lateral funiculus rostra1 to the recorded cell had constant latencies and decay phases which followed a single exponential with a time constant equal to the membrane time constant. These fe.s.ps were largely blocked by the non-NMDA glutamate receptor antagonist, 6-cyano-7-nitroquinoxaline (CNQX, 10-20 mM). Their amplitude increased with hyperpolarization and decreased with depolarization with no evidence of a slower NMDA-receptor mediated component. In transverse slices, stimulation of the lateral funiculus

With block of both glycine and GABAA receptors in slice

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352 McLACHLAN

or near the dorsal root entry zone can elicit polysynaptic fe.s.ps of longer time course which are sensitive to APV (33,34); this suggests that spinal but not supraspinal reflexes involve activation via NMDA receptors. At least part of the CNQX-insensitive component was inhibited by the P2x receptor antagonist, suramin (0.1-1 mM), which blocks some central excitatory synapses (35).

It was notable that gradual increases in stimulus strength in all cells produced a graded increase in fe.s.p. amplitude until threshold for the action potential was reached. Each individual axon thus produced an increment in the fe.s.p. of 5 1 mV, but large numbers of such axons were progressively recruited. Given the non-NMDA channel conductance of < 20 pS, very few channels must be activated by each recruited axon, i.e. each descending excitatory axon probably releases only a single quantum of glutamate. This might explain the smooth depolarization in in vivo recordings and suggests that the number of synaptic contacts made on a preganglionic neurone by any one descending axon is very low.

In a proportion of neurones, slow e.s.ps lasting > 5 seconds were evoked after the fe.s.p when high stimulus strengths were applied. As this response increased in amplitude with depolarization, decreased with hyperpolarization and was associated with an inward current of similar duration, it probably resulted from a decrease in membrane conductance to potassium ions. Such a conductance change could contribute to the progressive excitation during baroreceptor unloading

(19). Noradrenaline (NAd) is unlikely to be responsible for the slow e.s.p.

Its major action is to block the calcium-dependent conductances underlying the afterhyperpolarization. Action potentials initiated in NAd (10-100 mM) are followed by a burst of action potentials (36) and we have recorded a net inward current with a decay time constant of 150 ms under similar conditions. The discharge produced by NAd is much higher frequency than the discharge produced during the

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SYNAPTIC POTENTIALS IN VASOCONSTRICTOR PATHWAYS 353

baroreflex. On the other hand, 5-hydroxytryptamine is a potential candidate transmitter for the slow e.s.p as it produces a similar decrease in potassium conductance (37) and does not affect the afterhyperpol- arization.

PosteanElionic Neurones The properties of sympathetic postganglionic neurones have been

described using the same techniques in isolated paravertebral ganglia (31, 38)(see Table). These neurones also have low resting conductance and dendrites with a high impedance and short electrotonic length. As the ranges of values for cell capacitance are similar between pre- and postganglionic neurones (see Table), their membrane surface areas must be similar. Mean input resistance of postganglionic neurones is slightly lower than that of preganglionic neurones. Postganglionic neurones generally have only one slow calcium-activated potassium conductance corresponding to the faster of the two present in preganglionic neurones; this results in an afterhyperpolarization lasting some 500 ms. In many paravertebral neurones (31), this conductance is small so that the afterhyperpolarization will not necessarily limit the interspike interval.

Synaptic activation of paravertebral neurones (and prevertebral neurones projecting to vascular targets) using graded stimulation of the incoming preganglionic axons produces a series of distinct responses. As mentioned above, no inhibitory events are recorded but fe.s.ps of variable amplitude are evoked from up to about 10 preganglionic axons. Subthreshold fe.s.ps range from a few mV up to near threshold amplitudes; during repetitive activation at frequencies >0.5 Hz, these inputs show marked facilitation and may reach threshold (39). Characteristically, one (rarely two) of the preganglionic inputs to paravertebral ganglion cells of most species evoke a very large fe.s.p. which is always suprathreshold. This input is known as a strong fibre - like the motor axon at the skeletal neuromuscular junction, sufficient numbers of quanta of the transmitter are released by an impulse to

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354 McLACHLAN

ensure that an action potential is initiated in the postganglionic cell (38). When the membrane is hyperpolarized so as to block the action potential, the amplitude of the fe.s.p. may be > 50 mV. This underlying "synaptic potential" differs from the other subthreshold (weuk) inputs in that it has a fast component at its peak and the decay phase does not follow a single exponential (40). If the strong fibre is active during a reflex response, the centrally-derived signal is transmitted across the ganglion directly to the neurovascular junction. This relay is so effective that it would be difficult to distinguish an impulse synaptically transmitted across the ganglion from a direct connection in a classical fibre recording experiment. Strong fibre activity can clearly be distinguished in recordings from ganglion cells in vivo from action potentials arising from summation of 7ueak inputs (Fig. 1).

In vivo, the same reflex responses can be detected at both pre and postganglionic levels and the mean discharge frequency in axons of both types is low. Thus the strong pathway could be the only one which is effective in vasoconstrictor pathways. However, we do not know if different preganglionic inputs are involved in specific reflex responses. One idea is that synchronization of activity of subgroups of preganglionic neurones occurs within the spinal cord (41) but evidence for this has yet to be presented. How the synaptic connections within sympathetic ganglia contribute during natural activity is only beginning to be clarified.

CONCLUSION The vasoconstrictor system, because of its ubiquity and major role in

superficial muscle and skin, is accessible for experimental study of its electrical activity in humans (1, 2). Reflex responses during physiological adjustments including thermoregulation have been analysed. It has also been possible to examine the major effect of emotional responses on the cutaneous vasoconstrictor system (42). Changes in activity parallel changes in conductance of peripheral vascular beds.

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SYNAPTIC POTENTIALS IN VASOCONSTRICTOR PATHWAYS 355

Studies in anaesthetized animals and in isolated preparations have demonstrated that the preganglionic discharge pattern controlling vasoconstriction results from integration of many central subsystems. Within sympathetic ganglia, neurones with vasoconstrictor function receive relatively few inputs, at least one of which could transfer the preganglionic signal directly. When and how summation of the other convergent subthreshold inputs contributes to the vasoconstrictor signal has yet to be examined.

ACKNOWLEDGMENTS

This work has been supported by the National Health & Medical Research Council of Australia. I am grateful to my colleagues who have contributed to these studies and particularly to Dr. Pankaj Sah for the data from preganglionic neurones.

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