Three electrophysiological classes of guinea pig sympathetic postganglionic neurone have distinct morphologies

Abstract

Sympathetic postganglionic neurones can be differentiated electrophysiologically into three classes (phasic, Ph; tonic, T; and long-afterhyperpolarising, LAH) based on their potassium channel expression and consequent differences in excitability. We tested whether neuronal morphology differs between these classes. Neurones in coeliac, inferior mesenteric, and lower lumbar paravertebral ganglia of guinea pigs were filled with biocytin during in vitro experiments in which electrical properties were recorded. The dimensions of somata and dendrites were measured in approximately equal numbers of stained neurones of each class. The three electrophysiological classes were distinct in terms of soma shape, soma size (Ph < T = LAH), total dendritic length (LAH < Ph < T) and average length of dendrites (LAH < Ph < T) (P < 0.0001, multivariate analysis of variance). The mean number of primary dendrites also differed (LAH 13, Ph 16, T 20). The majority of dendrites did not branch, the ratios of terminations to primary dendrites being 1.36 (LAH), 1.63 (Ph) and 1.81 (T). Overall, LAH neurones, with medium-sized somata but the smallest dendritic trees, were more distinct morphologically than Ph and T neurones. The morphological differences between classes were not dependent on differences in location. Further, there was no apparent relation between morphology and the pattern of synaptic input each class receives. The results indicate that three distinct groups of sympathetic postganglionic neurone exist in adult guinea pigs, although more than three functions are subserved by these neurones.

Structure of peripheral synapses: autonomic ganglia

“…In contrast, quantitative analyses of dye-filled neurons in guinea-pig prevertebral sympathetic ganglia reveal that neurons in the prevertebral ganglia with intestinofugal inputs have dendritic field sizes about three times larger than neurons that receive only spinal preganglionic inputs (Boyd et al 1996;Anderson et al 2001). Furthermore, the average spatial density of preganglionic synapses onto neurons with intestinofugal inputs is similar to that of neurons without intestinofugal inputs (Gibbins et al 2003a).…”

“…Therefore, it is surprising that the size of presynaptic zones, the occurence of multiple presynaptic specialisations and the numbers of vesicles of preganglionic and intestinofugal synapses to coeliac ganglion neurons all are greater compared with preganglionic synapses to paravertebral ganglion neurons (Figs. 2a-c,f, 1b; Table 1), even Table 1 Synaptic organisation of sympathetic neurons in guinea-pigs (mean data derived from: Boyd et al 1996;Gibbins et al (1998Gibbins et al ( , 2003a though synaptic strength is generally greater in the latter. Even intestinofugal inputs with undetectable SNAP-25 immunoreactivity have large presynaptic densities compared with those in paravertebral ganglia (Fig.…”

“…They can be seen easily on the surface of dye-filled neurons (e.g. Boyd et al 1996;Gibbins and Matthew 1996;Gibbins et al 1998Gibbins et al , 2003a. Sometimes, the synapses seem to be directed to the process itself but, in other cases, the synaptic specialisation is directed to the base of the process or to the neuronal surface adjacent to the base of the process ( Fig.…”

Stereological and allometric studies on neurons and axo-dendritic synapses in the superior cervical ganglia of rats, capybaras and horses

“…clusters of two types of vesicles (agranular and granular) directed towards a well-defined density on a presynaptic membrane. Sometimes, the synapses seem to be directed to the dendritic spine itself, although the synaptic specialisation may also be found at the base of the spine or on the neuronal surface adjacent to the base of the dendritic spine (Matthews 1983;Boyd et al 1996;Gibbins and Matthew 1996;Gibbins et al 1998Gibbins et al , 2003.…”

Transmission of signals through sympathetic ganglia – modulation, integration or simply distribution?

“…Nevertheless, there is clearly a link between dendritic complexity and the number of innervating axons (Boyd et al 1996, Gibbins et al 1998). In particular, one class of prevertebral neurone (tonic rather than phasic in its discharge pattern) has more dendrites than the rest, and also receives more convergent inputs.…”