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Sympathetic Preganglionic Neurons: Properties and Inputs

Susan A. Deuchars, Varinder K. Lall

10.1002/cphy.c140020

Source: Volume 5, Issue 2, April 2015

Published online: March 2015

Full Article on Wiley Online Library



ABSTRACT

The sympathetic nervous system comprises one half of the autonomic nervous system and participates in maintaining homeostasis and enabling organisms to respond in an appropriate manner to perturbations in their environment, either internal or external. The sympathetic preganglionic neurons (SPNs) lie within the spinal cord and their axons traverse the ventral horn to exit in ventral roots where they form synapses onto postganglionic neurons. Thus, these neurons are the last point at which the central nervous system can exert an effect to enable changes in sympathetic outflow. This review considers the degree of complexity of sympathetic control occurring at the level of the spinal cord. The morphology and targets of SPNs illustrate the diversity within this group, as do their diverse intrinsic properties which reveal some functional significance of these properties. SPNs show high degrees of coupled activity, mediated through gap junctions, that enables rapid and coordinated responses; these gap junctions contribute to the rhythmic activity so critical to sympathetic outflow. The main inputs onto SPNs are considered; these comprise afferent, descending, and interneuronal influences that themselves enable functionally appropriate changes in SPN activity. The complexity of inputs is further demonstrated by the plethora of receptors that mediate the different responses in SPNs; their origins and effects are plentiful and diverse. Together these different inputs and the intrinsic and coupled activity of SPNs result in the rhythmic nature of sympathetic outflow from the spinal cord, which has a variety of frequencies that can be altered in different conditions. © 2015 American Physiological Society. Compr Physiol 5:829‐869, 2015.

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Figure 1. Figure 1. Overview of inputs and outputs of SPNs. SPNs synapse on sympathetic postganglionic neurons, which themselves synapse on the target organ, enabling reflex adjustments of the internal environment. Sensory information is conveyed to the thoracolumbar spinal cord by afferents with their somata in the dorsal root ganglion. Afferents communicate with SPNs in the spinal cord via local interneurons. Afferents additionally synapse onto ascending neurons which communicate with autonomic, limbic, and endocrine circuits in the brainstem and forebrain. Supraspinal pathways provide extensive innervation of SPNs. This enables higher order, integrative responses to changes in the internal environment. SPN: sympathetic preganglionic neuron; SPGN: sympathetic postganglionic neuron; DRG: dorsal root ganglion.
Figure 2. Figure 2. Autonomic nuclei in the spinal cord. (A) Spinal cord section with immunohistochemical identification of cholinergic SPNs and ventral horn motoneurons (using an antibody to choline acetyltransferase). (B) Line diagram of a transverse section of spinal cord showing the four groups of SPNs DH: dorsal horn; IML: intermediolateral cell column (nucleus intermediolateralis thoracolumbalis pars principalis); Ilf: nucleus intermediolateralis pars funicularis; IC: intercalated nucleus (nucleus intercalatus); IPPe: central autonomic area (nucleus intercalatus pars paraependymalis); VHMNs: ventral horn motoneurons.
Figure 3. Figure 3. Longitudinal section of mouse spinal cord with immunohistochemical labeling of SPNs using NADPH diaphorase which enables good dendritic visualization. Main picture at low magnification shows the different groups of SPNs with each panel illustrating the dendritic arborizations of each group of SPN. IML: intermediolateral cell column (nucleus intermediolateralis thoracolumbalis pars principalis); Ilf: nucleus intermediolateralis pars funicularis; IC: intercalated nucleus (nucleus intercalatus); IPPe: central autonomic area (nucleus intercalatus pars paraependymalis).
Figure 4. Figure 4. Target‐specific location of SPNs. (A) Transverse sections of the upper thoracic spinal cord of the adult rat at the T3 segmental level showing SCG‐SPN labeled with Fluorogold (bright gold) and SG‐SPN labeled with Fast Blue (bright blue). The groups of neurons have discrete occupancies in the IML. IML: nucleus intermediolateralis pars principalis; Ilf: nucleus intermediolateralis pars funicularis; DH: dorsal horn. (B) Diagram of the gray matter of the right side of spinal cord indicating the location in the IML of the different groups of SPN as they would appear at T5 thoracic segment. SCG: SPN projecting to superior cervical ganglion; SG: SPN projecting to stellate ganglion; SCG + SG: region containing both groups of SPN; AM: SPN projecting to the adrenal medulla. At more rostral levels, there would be very little AM representation whereas at more caudal levels such as T10 there would be very little representation of SG and no SCG. Adapted, with permission, from Pyner and Coote 1994 (301) Abbreviations: AM: adrenal medulla; SCG: superior cervical ganglion; SG: stellate ganglion.
Figure 5. Figure 5. Segmental localizationof SPNs projecting to different targets. (A) Photomicrograph of transverse spinal cord section in rats following pseudorabies (PRV) injection into the left kidney and a 4‐day survival postinfection. Arrows indicate the processes of infected neurons in the IML. (B) Number of PRV‐infected neurons in each segment 4 days after kidney infection. The arrow indicates the spinal cord segment that contains the most infected cells. Abbreviations: IML: the intermediolateral nucleus; LF: the lateral funiculus; IC: the intercalated nucleus; CA: central autonomic area. Adapted, with permission, from Huang and Weiss (137). (C) Summary of levels in the spinal cord where PRV‐infected SPNs were located following PRV injections into various end organs. Data used, with permission, from (50,105,106,226,227,228,283,313,338,341,346,358,359,368,369,370).
Figure 6. Figure 6. Nitric oxide synthase (NOS) is found in select groups of SPNs retrogradely labeled from the adrenal medulla (AM), superior cervical ganglion (SCG), coeliac ganglion (CG), and major pelvic ganglion (MPG). (A and B) SPN that project to the AM (arrows) contain NOS immunoreactivity. (C and D) SPN that project to the SCG (arrows) from the ventral IML (vIML) lack NOS immunoreactivity. (E and F) A sympathoadrenal neuron in the dorsolateral funiculus (DLF) that is NOS positive. (G and H) Most of the SPN that project to the MPG from the CAA are NOS positive (arrows) but one MPG‐projecting SPN (arrowhead) is NOS negative. (I and J) NOS‐immunoreactive SPN that send axons to the MPG (arrows) from the intercalated nucleus (ICN). (K and L) An NOS‐negative SPN (arrow) that supplies the CG from the ICN. A nearby NOS‐immunoreactive (arrowhead) neuron is not retrogradely labeled. (M and N) An NOS‐negative SPN that projects to the SCG from the central autonomic area (CAA) lies near a group of NOS‐positive CAA neurons that are not retrogradely labeled. Scale bars = 25 μm. Taken, with permission, from Hinrichs and Llewellyn‐Smith (131).
Figure 7. Figure 7. Neurochemical coding of SPNs innervating the adrenal or coeliac ganglia and activated by glucoprivation Using cFos immunoreactivity to label SPNs activated by glucoprivation (A), the retrograde tracer CTB conjugated to different fluorescent labels to retrogradely label either adrenal projecting (B) or coeliac projecting (C) SPN and in situ hybridization to show the presence of mRNA for preproenkephalin (D) it is clear that some of the activated SPN that project to these target organs are enkephalinergic [arrows in merged image (E)]. The group data are shown in F. Taken, with permission, from Parker et al. (285).
Figure 8. Figure 8. Properties of adrenal medulla‐projecting SPNs. (A) Longitudinal section of thoracolumbar spinal cord showing the distribution of SPN innervating the adrenal medulla as revealed by retrograde labeling of SPN with Rhodamine Dextran Lysine (RDL). [B(a)]) Transverse section of thoracic spinal cord showing SPNs labeled with RDL after injection into the adrenal medulla. The neuron indicated with the arrow in (a) was also filled (b) with Lucifer Yellow (LY) from the recording pipette, identifying its axonal projection to the adrenal medulla. Note another LY‐labeled neuron that lacked RDL, therefore not considered among the AD‐SPN population data. (C) Frequency histograms summarising the distribution of passive membrane properties of AD‐SPN. Top, resting membrane potentials (RMP; mV). Bottom, input resistances (MΩ). (D) Whole‐cell current‐clamp recordings (holding potential −50 mV) illustrate instantaneous inward rectification (*) activated during the membrane response to large amplitude hyperpolarising current pulses (not shown), and transient outward rectification (▪) observed as a delayed return to rest of the membrane responses. Also shown in the inset is an action potential on a faster time base to illustrate the pronounced shoulder on the repolarising phase (+). Adapted, with permission, from Wilson et al. (377).
Figure 9. Figure 9. Gap junctions in SPNs (A) The schematic shows the components of the gap junctions. (B) Upper trace shows regular action potentials recorded from an SPN in rat spinal cord slice (7‐22 days). If the membrane potential is hyperpolarized, these subthreshold oscillations in membrane potential are observed. (C) With Qx314 in the patch pipette to block sodium action potentials in the recorded cell, SPNs in the rat spinal cord slice are antidromically activated, producing an action potential in an SPN which is coupled through gap junctions to the recorded SPN. The oscillation then observed in the recorded SPN is the filtered action potential passing through the gap junction. (D) Simultaneous recordings from two electrotonically coupled SPNs demonstrate conduction of membrane potential changes from cell 1 to cell 2. A series of rectangular‐wave current steps (amplitude, −160, −80, and 40 pA; duration, 800 ms) injected into cell 1 elicited corresponding membrane potential responses in both neurons. Recordings from the same pair of neurons also show conduction of membrane potential changes from cell 2 to cell 1, following injection of current steps (amplitude, −160, −80, and 40 pA; duration, 800 ms) into cell 2. Taken, with permission, from Logan et al. (210) (B and C) and Nolan et al. (274) (D).
Figure 10. Figure 10. Classification of SPNs in the cat according to their responses to noxious stimulation and degree of cardiac modulation. Recordings are from SPNs in the anesthetized cat and various stimuli applied. (A) This group I SPN (middle trace is extracellular action potentials recorded) was excited by noxious stimulation of the ear (black line, Ai) and had strong cardiac rhythmicity, as illustrated in the pulse triggered histogram (Aii). (B) This group II SPN was inhibited by noxious stimulation and showed no cardiac rhythmicity. PHR: phrenic nerve activity; n(8 ms)‐1: number of action potentials occurring in an 8 ms time period. Taken, with permission. from Boczek‐Funcke et al. (32).
Figure 11. Figure 11. Transneuronal labeling of neurons in the brain after injections of PRV into the right stellate ganglion of the rat. A. Line drawings of brain sections where dots denote labeled cells in the different regions. Bilateral labeling is observed. (B) Organization of neuropeptide and monoamine neurons projecting to the stellate SPNs. The width of the line denotes quantitative differences in this projection system but does not necessarily reflect the potency of the pathway Important Abbreviations Rpa: raphe pallidus; R Ob: raphe obscurus; RMg: raphe magnus; RVLM: rostral ventrolateral medulla; A5: noradrenergic cell group; LC: locus coerulus; PVN: paraventricular nucleus; AHN: anterior hypothalamic nucleus. Taken and adapted, with permission, from Jansen et al. (156).
Figure 12. Figure 12. Photostimulation of channelrhodopsin‐expressing RVLM neurons in the rat activates blood pressure, heart rate, and sympathetic nerve discharge. (A) The cardiovascular and sympathetic effects produced by photostimulation of the RVLM with pulsed laser light (20 Hz, 10 ms, and 9 mW). Traces from top to bottom represent arterial pressure (AP), heart rate (HR), integrated sympathetic nerve discharge (SND; rectified and integrated with 2 s time constant and expressed relative to resting discharge, 0% representing the value observed at saturation of the baroreflex and 100% the resting level), and raw SND. (B) A waveform average of rectified SND triggered by laser pulse onset. (C) The effects of photostimulation on neurons in the RVLM. Cells were grouped based on their sensitivity to laser light (LL) stimulation, those activated were silenced by elevated arterial pressure while those that were insensitive to LL were not. The grouped data from event‐triggered histograms (1 ms bin) from LL activated neurons demonstrated that during 20 Hz laser stimulation, virtually all action potentials (AP on y‐axis) occur within 10 ms of the laser pulse onset with a large peak occurring 5 ms after the onset of the laser pulse. A subsidiary peak occurred between 9 and 10 ms representing cases when cells fired in couplets. For comparison, the same averaging of LL‐insensitive cells shows no relationship with the timing of the laser pulse. The right panel shows that LL sensitive neurons (filled with biotinamide during recording) expressed channelrhodopsin while the insensitive cells did not. Taken, with permission, from Abbott et al. (2).
Figure 13. Figure 13. Effect of hypothermia and bicuculline microinjection into raphe pallidus (RPa) on sympathetic nerve activity to brown adipose tissue in anesthetized rat. Panels A and B are from same experiment. (A) AP, BAT SNA, and BAT SNA PWR during control conditions (colonic temperature: 37.5°C) and acute hypothermia (34.7°C). It is clear that BAT SNA is increased during hypothermia. (B) AP, BAT SNA, and HR responses to microinjection (arrow; 60 nL) of bicuculline (500 μmol/L) into RPa. (C) Immunocytochemical staining for Fos (used as an indicator of activated neurons) in neurons of midline brain stem after 4‐h exposure to environmental temperature of 4°C (cold) or 22°C (control). Note large increase in Fos expression in RPa at level of bregma −10.30 in animal exposed to acute hypothermia. Abbreviations: BAT SNA: sympathetic nerve activity to brown adipose tissue; BAT SNA PWR: autospectrum of BAT SNA; AP: arterial pressure; HR: heart rate; RPa: raphe pallidus. Adapted, with permission, from Morrison et al. (264).
Figure 14. Figure 14. Sympathetic interneurons in the rat spinal cord. (A) Top panel: low magnification photograph of a juxtacellularly labeled, sympathetically correlated neuron histologically located in lamina IV of the dorsal horn. Bottom panel: dark trace: cross‐correlation between the incidence of discharge of a sympathetically correlated dorsal horn interneuron and simultaneously recorded RSNA in the anaesthetized rat. Light traces: dummy cross correlations between RSNA and discharges of a simulated neuron. (B) Action potentials recorded from an SPN and an IML interneuron in rat spinal cord slices showing the faster repolarization phase of the interneuronal action potential. On the right, immunohistochemical analysis of Kv3.1b (top) combined with fluorogold labeling of SPNs (bottom) show that interneurons, not SPNs, express Kv3.1b. C. Filled IML interneuron (inset) and line drawing of the axonal and dendritic arborization. Adapted, with permission, from Tang et al. (354) (A) and Deuchars et al. (86) (B and C).
Figure 15. Figure 15. GABA and glutamate terminals influence SPNs in the rat. (A) Immunohistochemical localization of glutamate and GABA in terminals onto SPNs retrogradely labeled after injection into the superior cervical ganglion (reaction product arrowed). Small dots (10‐nm gold particles) are in glutamatergic terminals and larger dots (15‐nm gold particles) are in GABAergic terminals. It is clear that the two neurotransmitters do not colocalise‐in the top panel, only small particles are present in the terminal (glutamatergic) while in the bottom panel, only larger gold particles are located in the terminal (GABAergic). (B) Stimulation of the lateral funiculus elicits fast excitatory postsynaptic potentials which are blocked by the antagonists for excitatory amino acids (CNQX and AP‐5). (C) Ongoing inhibitory postsynaptic potentials in SPNs recorded in spinal cord slices. These are GABAergic since they are inhibited by bicuculline. Taken, with permission, from Llewellyn‐Smith et al. (195) (A), Deuchars et al. (85) (B), and Wang et al. (374) (C).
Figure 16. Figure 16. 5‐HT induces oscillatory activity in the IML. (A) Low‐pass filtered (<35 Hz) extracellular voltage recording from the IML of a single 500 micron rat spinal cord slice before (left) and after (right) application of 10 μmol/L 5‐HT. Rhythmic oscillations appear during 5‐HT application. (B) Power spectral analysis of a 1 min segment of control (left) and 5‐HT (right) activity showing a prominent peak at 9.4 Hz. (C) Autocorrelograms showing that the activity is self‐similar (rhythmic) only after 5‐HT is applied. (D) Surface plot of power spectra taken at consecutive time points from a different slice, showing the development and decline of an 11.9 Hz oscillation over time. (E) Bar chart of the mean data shows the mean oscillation frequency was not affected by 5‐HT (n = 5). Error bars = SEM. (F) Box plot of oscillation power. Ten micromole per liter 5‐HT significantly increased the power of the oscillation. *P < 0.05. Taken, with permission, from Pierce et al. (290).
Figure 17. Figure 17. Adenosine acts via two different receptors to produce an overall reduction in SPN excitability. (A) Electron microscopy of immunoreactivity for adenosine A1 receptor (Ai) or A2A receptor (Aii) in rat spinal cord IML. Open arrow points to the synapse, closed arrows point to the A1 or A2A reaction product and the dashed arrow points to the labeling of the SPN. Both A1 and A2A immunopositive terminals form synaptic contacts directly onto IML neurons. (B) Stimulation of the lateral funiculus in rat spinal cord slices elicits EPSPs which are reduced in amplitude by the A1R agonist CPA but not by the A2AR agonist CGS21680 (CGS). If EPSPs are blocked by the excitatory amino acid antagonists NBQX and AP‐5, IPSPs are revealed at depolarized potentials and these are not affected by A1R activation but are enhanced by A2AR activation. (C) Schematic showing the presence of A1 adenosine receptors on excitatory descending terminals which, when activated, reduce neurotransmitter release and A2A adenosine receptors on inhibitory descending terminals which act to enhance inhibitory transmission. Together adenosine acts via two receptors to produce an overall dampening of the SPN activity. Taken, with permission, from Deuchars et al. (85) (Ai) and Brooke et al. (38) (Aii, B, and C).
Figure 18. Figure 18. Physiologically relevant sympathetic rhythmic activity can be generated in the spinalized rat. Power density spectra of lumbar sympathetic nerve activity before (A) and after (B) transection of the spinal cord and after excitation of sympathetic activity by intrathecal injection of kainic acid (C). It is clear that sympathetic activity in the 2 to 6 Hz frequency range can be generated in the spinal cord, in the absence of supraspinal inputs. Taken, with permission, from Allen et al. (4).


Figure 1. Overview of inputs and outputs of SPNs. SPNs synapse on sympathetic postganglionic neurons, which themselves synapse on the target organ, enabling reflex adjustments of the internal environment. Sensory information is conveyed to the thoracolumbar spinal cord by afferents with their somata in the dorsal root ganglion. Afferents communicate with SPNs in the spinal cord via local interneurons. Afferents additionally synapse onto ascending neurons which communicate with autonomic, limbic, and endocrine circuits in the brainstem and forebrain. Supraspinal pathways provide extensive innervation of SPNs. This enables higher order, integrative responses to changes in the internal environment. SPN: sympathetic preganglionic neuron; SPGN: sympathetic postganglionic neuron; DRG: dorsal root ganglion.


Figure 2. Autonomic nuclei in the spinal cord. (A) Spinal cord section with immunohistochemical identification of cholinergic SPNs and ventral horn motoneurons (using an antibody to choline acetyltransferase). (B) Line diagram of a transverse section of spinal cord showing the four groups of SPNs DH: dorsal horn; IML: intermediolateral cell column (nucleus intermediolateralis thoracolumbalis pars principalis); Ilf: nucleus intermediolateralis pars funicularis; IC: intercalated nucleus (nucleus intercalatus); IPPe: central autonomic area (nucleus intercalatus pars paraependymalis); VHMNs: ventral horn motoneurons.


Figure 3. Longitudinal section of mouse spinal cord with immunohistochemical labeling of SPNs using NADPH diaphorase which enables good dendritic visualization. Main picture at low magnification shows the different groups of SPNs with each panel illustrating the dendritic arborizations of each group of SPN. IML: intermediolateral cell column (nucleus intermediolateralis thoracolumbalis pars principalis); Ilf: nucleus intermediolateralis pars funicularis; IC: intercalated nucleus (nucleus intercalatus); IPPe: central autonomic area (nucleus intercalatus pars paraependymalis).


Figure 4. Target‐specific location of SPNs. (A) Transverse sections of the upper thoracic spinal cord of the adult rat at the T3 segmental level showing SCG‐SPN labeled with Fluorogold (bright gold) and SG‐SPN labeled with Fast Blue (bright blue). The groups of neurons have discrete occupancies in the IML. IML: nucleus intermediolateralis pars principalis; Ilf: nucleus intermediolateralis pars funicularis; DH: dorsal horn. (B) Diagram of the gray matter of the right side of spinal cord indicating the location in the IML of the different groups of SPN as they would appear at T5 thoracic segment. SCG: SPN projecting to superior cervical ganglion; SG: SPN projecting to stellate ganglion; SCG + SG: region containing both groups of SPN; AM: SPN projecting to the adrenal medulla. At more rostral levels, there would be very little AM representation whereas at more caudal levels such as T10 there would be very little representation of SG and no SCG. Adapted, with permission, from Pyner and Coote 1994 (301) Abbreviations: AM: adrenal medulla; SCG: superior cervical ganglion; SG: stellate ganglion.


Figure 5. Segmental localizationof SPNs projecting to different targets. (A) Photomicrograph of transverse spinal cord section in rats following pseudorabies (PRV) injection into the left kidney and a 4‐day survival postinfection. Arrows indicate the processes of infected neurons in the IML. (B) Number of PRV‐infected neurons in each segment 4 days after kidney infection. The arrow indicates the spinal cord segment that contains the most infected cells. Abbreviations: IML: the intermediolateral nucleus; LF: the lateral funiculus; IC: the intercalated nucleus; CA: central autonomic area. Adapted, with permission, from Huang and Weiss (137). (C) Summary of levels in the spinal cord where PRV‐infected SPNs were located following PRV injections into various end organs. Data used, with permission, from (50,105,106,226,227,228,283,313,338,341,346,358,359,368,369,370).


Figure 6. Nitric oxide synthase (NOS) is found in select groups of SPNs retrogradely labeled from the adrenal medulla (AM), superior cervical ganglion (SCG), coeliac ganglion (CG), and major pelvic ganglion (MPG). (A and B) SPN that project to the AM (arrows) contain NOS immunoreactivity. (C and D) SPN that project to the SCG (arrows) from the ventral IML (vIML) lack NOS immunoreactivity. (E and F) A sympathoadrenal neuron in the dorsolateral funiculus (DLF) that is NOS positive. (G and H) Most of the SPN that project to the MPG from the CAA are NOS positive (arrows) but one MPG‐projecting SPN (arrowhead) is NOS negative. (I and J) NOS‐immunoreactive SPN that send axons to the MPG (arrows) from the intercalated nucleus (ICN). (K and L) An NOS‐negative SPN (arrow) that supplies the CG from the ICN. A nearby NOS‐immunoreactive (arrowhead) neuron is not retrogradely labeled. (M and N) An NOS‐negative SPN that projects to the SCG from the central autonomic area (CAA) lies near a group of NOS‐positive CAA neurons that are not retrogradely labeled. Scale bars = 25 μm. Taken, with permission, from Hinrichs and Llewellyn‐Smith (131).


Figure 7. Neurochemical coding of SPNs innervating the adrenal or coeliac ganglia and activated by glucoprivation Using cFos immunoreactivity to label SPNs activated by glucoprivation (A), the retrograde tracer CTB conjugated to different fluorescent labels to retrogradely label either adrenal projecting (B) or coeliac projecting (C) SPN and in situ hybridization to show the presence of mRNA for preproenkephalin (D) it is clear that some of the activated SPN that project to these target organs are enkephalinergic [arrows in merged image (E)]. The group data are shown in F. Taken, with permission, from Parker et al. (285).


Figure 8. Properties of adrenal medulla‐projecting SPNs. (A) Longitudinal section of thoracolumbar spinal cord showing the distribution of SPN innervating the adrenal medulla as revealed by retrograde labeling of SPN with Rhodamine Dextran Lysine (RDL). [B(a)]) Transverse section of thoracic spinal cord showing SPNs labeled with RDL after injection into the adrenal medulla. The neuron indicated with the arrow in (a) was also filled (b) with Lucifer Yellow (LY) from the recording pipette, identifying its axonal projection to the adrenal medulla. Note another LY‐labeled neuron that lacked RDL, therefore not considered among the AD‐SPN population data. (C) Frequency histograms summarising the distribution of passive membrane properties of AD‐SPN. Top, resting membrane potentials (RMP; mV). Bottom, input resistances (MΩ). (D) Whole‐cell current‐clamp recordings (holding potential −50 mV) illustrate instantaneous inward rectification (*) activated during the membrane response to large amplitude hyperpolarising current pulses (not shown), and transient outward rectification (▪) observed as a delayed return to rest of the membrane responses. Also shown in the inset is an action potential on a faster time base to illustrate the pronounced shoulder on the repolarising phase (+). Adapted, with permission, from Wilson et al. (377).


Figure 9. Gap junctions in SPNs (A) The schematic shows the components of the gap junctions. (B) Upper trace shows regular action potentials recorded from an SPN in rat spinal cord slice (7‐22 days). If the membrane potential is hyperpolarized, these subthreshold oscillations in membrane potential are observed. (C) With Qx314 in the patch pipette to block sodium action potentials in the recorded cell, SPNs in the rat spinal cord slice are antidromically activated, producing an action potential in an SPN which is coupled through gap junctions to the recorded SPN. The oscillation then observed in the recorded SPN is the filtered action potential passing through the gap junction. (D) Simultaneous recordings from two electrotonically coupled SPNs demonstrate conduction of membrane potential changes from cell 1 to cell 2. A series of rectangular‐wave current steps (amplitude, −160, −80, and 40 pA; duration, 800 ms) injected into cell 1 elicited corresponding membrane potential responses in both neurons. Recordings from the same pair of neurons also show conduction of membrane potential changes from cell 2 to cell 1, following injection of current steps (amplitude, −160, −80, and 40 pA; duration, 800 ms) into cell 2. Taken, with permission, from Logan et al. (210) (B and C) and Nolan et al. (274) (D).


Figure 10. Classification of SPNs in the cat according to their responses to noxious stimulation and degree of cardiac modulation. Recordings are from SPNs in the anesthetized cat and various stimuli applied. (A) This group I SPN (middle trace is extracellular action potentials recorded) was excited by noxious stimulation of the ear (black line, Ai) and had strong cardiac rhythmicity, as illustrated in the pulse triggered histogram (Aii). (B) This group II SPN was inhibited by noxious stimulation and showed no cardiac rhythmicity. PHR: phrenic nerve activity; n(8 ms)‐1: number of action potentials occurring in an 8 ms time period. Taken, with permission. from Boczek‐Funcke et al. (32).


Figure 11. Transneuronal labeling of neurons in the brain after injections of PRV into the right stellate ganglion of the rat. A. Line drawings of brain sections where dots denote labeled cells in the different regions. Bilateral labeling is observed. (B) Organization of neuropeptide and monoamine neurons projecting to the stellate SPNs. The width of the line denotes quantitative differences in this projection system but does not necessarily reflect the potency of the pathway Important Abbreviations Rpa: raphe pallidus; R Ob: raphe obscurus; RMg: raphe magnus; RVLM: rostral ventrolateral medulla; A5: noradrenergic cell group; LC: locus coerulus; PVN: paraventricular nucleus; AHN: anterior hypothalamic nucleus. Taken and adapted, with permission, from Jansen et al. (156).


Figure 12. Photostimulation of channelrhodopsin‐expressing RVLM neurons in the rat activates blood pressure, heart rate, and sympathetic nerve discharge. (A) The cardiovascular and sympathetic effects produced by photostimulation of the RVLM with pulsed laser light (20 Hz, 10 ms, and 9 mW). Traces from top to bottom represent arterial pressure (AP), heart rate (HR), integrated sympathetic nerve discharge (SND; rectified and integrated with 2 s time constant and expressed relative to resting discharge, 0% representing the value observed at saturation of the baroreflex and 100% the resting level), and raw SND. (B) A waveform average of rectified SND triggered by laser pulse onset. (C) The effects of photostimulation on neurons in the RVLM. Cells were grouped based on their sensitivity to laser light (LL) stimulation, those activated were silenced by elevated arterial pressure while those that were insensitive to LL were not. The grouped data from event‐triggered histograms (1 ms bin) from LL activated neurons demonstrated that during 20 Hz laser stimulation, virtually all action potentials (AP on y‐axis) occur within 10 ms of the laser pulse onset with a large peak occurring 5 ms after the onset of the laser pulse. A subsidiary peak occurred between 9 and 10 ms representing cases when cells fired in couplets. For comparison, the same averaging of LL‐insensitive cells shows no relationship with the timing of the laser pulse. The right panel shows that LL sensitive neurons (filled with biotinamide during recording) expressed channelrhodopsin while the insensitive cells did not. Taken, with permission, from Abbott et al. (2).


Figure 13. Effect of hypothermia and bicuculline microinjection into raphe pallidus (RPa) on sympathetic nerve activity to brown adipose tissue in anesthetized rat. Panels A and B are from same experiment. (A) AP, BAT SNA, and BAT SNA PWR during control conditions (colonic temperature: 37.5°C) and acute hypothermia (34.7°C). It is clear that BAT SNA is increased during hypothermia. (B) AP, BAT SNA, and HR responses to microinjection (arrow; 60 nL) of bicuculline (500 μmol/L) into RPa. (C) Immunocytochemical staining for Fos (used as an indicator of activated neurons) in neurons of midline brain stem after 4‐h exposure to environmental temperature of 4°C (cold) or 22°C (control). Note large increase in Fos expression in RPa at level of bregma −10.30 in animal exposed to acute hypothermia. Abbreviations: BAT SNA: sympathetic nerve activity to brown adipose tissue; BAT SNA PWR: autospectrum of BAT SNA; AP: arterial pressure; HR: heart rate; RPa: raphe pallidus. Adapted, with permission, from Morrison et al. (264).


Figure 14. Sympathetic interneurons in the rat spinal cord. (A) Top panel: low magnification photograph of a juxtacellularly labeled, sympathetically correlated neuron histologically located in lamina IV of the dorsal horn. Bottom panel: dark trace: cross‐correlation between the incidence of discharge of a sympathetically correlated dorsal horn interneuron and simultaneously recorded RSNA in the anaesthetized rat. Light traces: dummy cross correlations between RSNA and discharges of a simulated neuron. (B) Action potentials recorded from an SPN and an IML interneuron in rat spinal cord slices showing the faster repolarization phase of the interneuronal action potential. On the right, immunohistochemical analysis of Kv3.1b (top) combined with fluorogold labeling of SPNs (bottom) show that interneurons, not SPNs, express Kv3.1b. C. Filled IML interneuron (inset) and line drawing of the axonal and dendritic arborization. Adapted, with permission, from Tang et al. (354) (A) and Deuchars et al. (86) (B and C).


Figure 15. GABA and glutamate terminals influence SPNs in the rat. (A) Immunohistochemical localization of glutamate and GABA in terminals onto SPNs retrogradely labeled after injection into the superior cervical ganglion (reaction product arrowed). Small dots (10‐nm gold particles) are in glutamatergic terminals and larger dots (15‐nm gold particles) are in GABAergic terminals. It is clear that the two neurotransmitters do not colocalise‐in the top panel, only small particles are present in the terminal (glutamatergic) while in the bottom panel, only larger gold particles are located in the terminal (GABAergic). (B) Stimulation of the lateral funiculus elicits fast excitatory postsynaptic potentials which are blocked by the antagonists for excitatory amino acids (CNQX and AP‐5). (C) Ongoing inhibitory postsynaptic potentials in SPNs recorded in spinal cord slices. These are GABAergic since they are inhibited by bicuculline. Taken, with permission, from Llewellyn‐Smith et al. (195) (A), Deuchars et al. (85) (B), and Wang et al. (374) (C).


Figure 16. 5‐HT induces oscillatory activity in the IML. (A) Low‐pass filtered (<35 Hz) extracellular voltage recording from the IML of a single 500 micron rat spinal cord slice before (left) and after (right) application of 10 μmol/L 5‐HT. Rhythmic oscillations appear during 5‐HT application. (B) Power spectral analysis of a 1 min segment of control (left) and 5‐HT (right) activity showing a prominent peak at 9.4 Hz. (C) Autocorrelograms showing that the activity is self‐similar (rhythmic) only after 5‐HT is applied. (D) Surface plot of power spectra taken at consecutive time points from a different slice, showing the development and decline of an 11.9 Hz oscillation over time. (E) Bar chart of the mean data shows the mean oscillation frequency was not affected by 5‐HT (n = 5). Error bars = SEM. (F) Box plot of oscillation power. Ten micromole per liter 5‐HT significantly increased the power of the oscillation. *P < 0.05. Taken, with permission, from Pierce et al. (290).


Figure 17. Adenosine acts via two different receptors to produce an overall reduction in SPN excitability. (A) Electron microscopy of immunoreactivity for adenosine A1 receptor (Ai) or A2A receptor (Aii) in rat spinal cord IML. Open arrow points to the synapse, closed arrows point to the A1 or A2A reaction product and the dashed arrow points to the labeling of the SPN. Both A1 and A2A immunopositive terminals form synaptic contacts directly onto IML neurons. (B) Stimulation of the lateral funiculus in rat spinal cord slices elicits EPSPs which are reduced in amplitude by the A1R agonist CPA but not by the A2AR agonist CGS21680 (CGS). If EPSPs are blocked by the excitatory amino acid antagonists NBQX and AP‐5, IPSPs are revealed at depolarized potentials and these are not affected by A1R activation but are enhanced by A2AR activation. (C) Schematic showing the presence of A1 adenosine receptors on excitatory descending terminals which, when activated, reduce neurotransmitter release and A2A adenosine receptors on inhibitory descending terminals which act to enhance inhibitory transmission. Together adenosine acts via two receptors to produce an overall dampening of the SPN activity. Taken, with permission, from Deuchars et al. (85) (Ai) and Brooke et al. (38) (Aii, B, and C).


Figure 18. Physiologically relevant sympathetic rhythmic activity can be generated in the spinalized rat. Power density spectra of lumbar sympathetic nerve activity before (A) and after (B) transection of the spinal cord and after excitation of sympathetic activity by intrathecal injection of kainic acid (C). It is clear that sympathetic activity in the 2 to 6 Hz frequency range can be generated in the spinal cord, in the absence of supraspinal inputs. Taken, with permission, from Allen et al. (4).
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Article Title: Sympathetic Preganglionic Neurons: Properties and Inputs
 

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Susan A. Deuchars, Varinder K. Lall. Sympathetic Preganglionic Neurons: Properties and Inputs. Compr Physiol 2015, 5: 829-869. doi: 10.1002/cphy.c140020