Innervate Ganglion Cells Research Articles

Quantitative relationships between taste bud development and gustatory ganglion cells.

To determine whether patterns of taste bud innervation change during postnatal rat development, the number of geniculate ganglion cells that innervate single taste buds were quantified in adult and developing rats. While there was a large variation in numbers of ganglion cells that innervate individual taste buds, there was a high degree of organization in the system. Namely, the number of labeled geniculate ganglion cells innervating a taste bud was highly correlated with the size of the taste bud. This relationship between taste bud size and number of innervating ganglion cells develops over a prolonged postnatal period and is not established until postnatal day 40 (P40), when taste buds reach their adult size. In a second series of experiments, we sought to determine whether neural rearrangement of chorda tympani neurons is responsible for the development of this relationship by double-labeling single taste buds at different ages. We found that the number of ganglion cells innervating individual taste buds on P10 predicts the size that taste buds become by P40. This finding suggests that neural rearrangement is not responsible for establishing the relationship between taste bud size and the number of innervating ganglion cells during development. More importantly, it strongly suggests that the 'neural template' for the mature innervation pattern is determined during early postnatal development.

Innervation of single fungiform taste buds during development in rat

To determine whether the innervation of taste buds changes during postnatal development, the number of geniculate ganglion cells that innervated single fungiform taste buds were quantified in the tip- and midregions of the tongue of adult and developing rats. There was substantial variation in both the size of individual taste buds and number of geniculate ganglion cells that innervated them. Importantly, taste bud morphology and innervation were highly related. Namely, the number of labeled geniculate ganglion cells that innervated a taste bud was highly correlated with the size of the taste bud (r = 0.91, P < .0003): The larger the taste bud, the more geniculate ganglion cells that innervated it. The relationship between ganglion cell number and taste bud volume emerged during the first 40 days postnatal. Whereas there was no difference in the average number of ganglion cells that innervated individual taste buds in rats aged 10 days postnatal through adulthood, taste bud volumes increased progressively between 10 and 40 days postnatal, at which age taste bud volumes were similar to adults. The maturation of taste bud size was accompanied by the emergence of the relationship between taste bud volume and number of innervating neurons. Specifically, there was no correlation between taste bud size and number of innervating geniculate ganglion cells in 10-, 20-, or 30-day-old rats, whereas taste bud size and the number of innervating ganglion cells in 40-day-old rats were positively correlated (r = .80, P < .002). Therefore, the relationship between taste bud size and number of innervating ganglion cells develops over a prolonged postnatal period and is established when taste buds grow to their adult size. J. Comp. Neurol. 398:13–24, 1998. © 1998 Wiley-Liss, Inc.

Innervation of single fungiform taste buds during development in rat

To determine whether the innervation of taste buds changes during postnatal development, the number of geniculate ganglion cells that innervated single fungiform taste buds were quantified in the tip- and midregions of the tongue of adult and developing rats. There was substantial variation in both the size of individual taste buds and number of geniculate ganglion cells that innervated them. Importantly, taste bud morphology and innervation were highly related. Namely, the number of labeled geniculate ganglion cells that innervated a taste bud was highly correlated with the size of the taste bud (r = 0.91, P < .0003): The larger the taste bud, the more geniculate ganglion cells that innervated it. The relationship between ganglion cell number and taste bud volume emerged during the first 40 days postnatal. Whereas there was no difference in the average number of ganglion cells that innervated individual taste buds in rats aged 10 days postnatal through adulthood, taste bud volumes increased progressively between 10 and 40 days postnatal, at which age taste bud volumes were similar to adults. The maturation of taste bud size was accompanied by the emergence of the relationship between taste bud volume and number of innervating neurons. Specifically, there was no correlation between taste bud size and number of innervating geniculate ganglion cells in 10-, 20-, or 30-day-old rats, whereas taste bud size and the number of innervating ganglion cells in 40-day-old rats were positively correlated (r = .80, P < .002). Therefore, the relationship between taste bud size and number of innervating ganglion cells develops over a prolonged postnatal period and is established when taste buds grow to their adult size.

Innervation Patterns in Congenital Biliary Dilatation*

The innervation of choledochal cysts was studied to see if the distribution of innervating ganglion cells can be utilized as a possible indicator of the damage and dilatation process of choledochus. Specimens from 32 patients aged 1 month to 12 years were stained by the immunoperoxidase method with neural tissue-specific antibodies, the innervating ganglion cells were counted and their number was correlated with the clinical severity, patient's age-at-surgery, and intraoperative cholangiographic and/or ERCP findings. In cystic dilatation, the total number of ganglion cells within the choledochal wall was significantly lower than in control specimens regardless of the diameter of the choledochal cyst, age-at-surgery, or clinical course. In fusiform dilatation, the total number of ganglion cells varied according to the severity of the clinical presentation, and the diameter of the fusiform choledochus increased in proportion to the patient's age-at-surgery. The distribution of innervating ganglion cells is thought to correlate quantitatively with the damage and dilatation process responsible for the choledochal cyst. These results may support a hypothesis that the pathogenesis of cystic dilatation proceeds antenatally or soon after birth, while that of fusiform dilatation begins after birth.

Peripheral target regulation of dendritic geometry in the rat superior cervical ganglion

Dendritic arborizations of neurons in the adult rat superior cervical ganglion were measured in control ganglia and in ganglia innervating peripheral targets that were relatively larger or smaller than normal. The relative size of the target--the submandibular gland in these experiments--was manipulated during development by changing the ratio between the amount of target tissue and the number of innervating ganglion cells. Thus, ligating the submandibular salivary duct reduced the size of the gland, whereas partially denervating the gland produced a relatively larger target by making a smaller number of ganglion cells innervate a gland of normal size. Neurons innervating targets that were smaller than normal had significantly smaller dendritic arborizations and cell bodies than control cells. Conversely, neurons projecting to relatively larger than normal targets had larger dendritic arborizations and cell bodies, and more primary dendritic branches. Such cells were also innervated by a larger than normal number of preganglionic inputs. A similar change in dendritic geometry was observed when relative target size was increased after cutting the cervical sympathetic trunk, showing that target regulation of dendritic geometry is not dependent on ganglion cell activity or the presence of presynaptic innervation. Dendrites in the superior cervical ganglion normally grow in parallel with body size throughout life (Purves et al., 1986a; Voyvodic, 1987a). The present results imply that an important aspect of dendritic growth is an ongoing responsiveness of ganglion cells to feedback signals arising from the peripheral targets they innervate.

Rostrocaudal differences in dendritic growth and synaptogenesis in rat sympathetic chain ganglia.

Vertebrate embryos show a rostral to caudal gradient of morphogenesis. I have investigated the effect of this developmental gradient on neuronal maturation and synapse formation by comparing the development of rostral and caudal sympathetic chain ganglia in the rat. In young adults the superior cervical and lumbar ganglia are almost identical in terms of neuronal morphology and quantitative aspects of innervation. In neonates, however, substantial rostrocaudal differences are apparent in dendritic complexity, number of axons innervating ganglion cells, and synaptic density. There is an associated delay in ganglion cell-target interactions in the lumbar region. My results show that rostrocaudal position is significantly correlated with the time course of dendritic growth and synaptogenesis and suggest that ganglion cell-target interactions may be important in these developmental processes. This difference in developmental rate, however, does not lead to differences in neuronal morphology or synaptic density between rostral and caudal ganglia in maturity.

The selective innervation of guinea-pig superior cervical ganglion cells by sprouts from intact preganglionic axons.

If the guinea-pig superior cervical ganglion is partially denervated in a way which spares some preganglionic axons arising from each of the spinal cord segments which normally innervate this ganglion (C8-T7), sprouting of the intact preganglionic axons occurs without a loss of selective end-organ responses to stimulation of individual ventral roots (Maehlen & Njå, 1981). In the present work we examine the selective innervation of individual ganglion cells by ventral roots after sprouting and compare it to that in normal ganglia. After sprouting the pattern of ganglion cell innervation by the intact preganglionic axons shows some of the features typical of normal ganglia. Thus each ganglion cell is strongly innervated by one or two neighbouring spinal cord segments, with the adjacent segments contributing a synaptic influence which diminishes with distance from the dominant one. Acutely after the partial denervation there is a tendency for the rostral segments to innervate ganglion cells more strongly than do caudal segments, compared to the situation in normal ganglia. The same is true following sprouting. The pattern of ganglion cell innervation observed after sprouting can be explained if the affinities of ganglion cells for innervation from particular spinal levels are assumed to be unchanged and the shift in the relative availability of different preganglionic axons, caused by the partial denervation, is taken into account. This view was substantiated by statistical analysis based on a model of selective synapse formation in the guinea-pig superior cervical ganglion. We conclude that the ability of individual ganglion cells to distinguish preganglionic axons arising from different spinal levels is maintained during sprouting. Moreover, the way in which selective recognition and the availability of different preganglionic axons combine to produce particular patterns of innervation appears to be similar in normal development and after partial denervation in maturity.

Apportionment of the terminals from single preganglionic axons to target neurones in the rabbit ciliary ganglion.

We have studied the apportionment of terminals from single preganglionic axons to target neurones in the ciliary ganglion of adult rabbits. Both electrical recording and intra-axonal injection of horseradish peroxidase (HRP) showed that each preganglionic axon innervates only a small fraction of the ganglion cell population (about 10-20 of the approximately 400 ganglion cells). Examination of ganglia in whole mounts showed that neurones whose cell bodies were enveloped by HRP-labelled boutons from a single axon were often surrounded by other neurones which received no contacts from the labelled fibre. Electron microscopical examination of labelled presynaptic terminals on individual ganglion cells confirmed that the boutons of single axons were sharply confined to particular target cells. This suggests that individual target neurones (or portions of them) are the unit of innervation during the development of these synaptic connexions. Comparison of the amplitudes of synaptic responses in singly and multiply innervated ganglion cells indicated that, on average, an individual axon made a weaker synaptic connexion with a multiply innervated neurone than with neurone that received only one input. Moreover, neurones innervated by several different axons tended to have fewer synapses on their somata than neurones innervated by only one or two preganglionic axons. Individual post-synaptic profiles were often contacted exclusively by labelled terminals when examined in the electron microscope. Since many of these neurones are multiply innervated, this observation suggests some regional separation of the several inputs contacting the same cell. For several reasons, however, this inference must be regarded as tentative. Taken together, these findings provide a possible explanation of the correlation between the dendritic geometry of ganglion cells and the number of different axons that innervate them (Purves & Hume, 1981). The several axons that initially innervate ganglion cells without dendrites evidently compete during early life until only a single input remains. On ganglion cells with dendrites, however, the number of inputs that persists is proportional to dendritic complexity. The present results suggest that the diminished competition between axons innervating neurones with dendrites may result from some degree of terminal segregation on dendritic arborizations.

On the purpose of selective innervation of guinea‐pig superior cervical ganglion cells.

Preganglionic axons arising from different levels of the mammalian spinal cord make preferential connexions with different classes of superior cervical ganglion cells (Langley, 1892, 1900; Njå & Purves, 1977a). For example, preganglionic axons from the first thoracic segment (T1) make relatively strong connexions with ganglion cells activating end-organs of the eye; conversely, axons arising from T4 selectively innervate ganglion cells projecting to the ear. In the present work we have asked whether this selectivity reflects the function of the pre- and post-synaptic cells, and aspect of their respective positions, or some other criterion. 1. End-organs with different functions at the same locus (the eye) respond to stimulation of the same ventral roots; end-organs of a single modality (hairs or blood vessels) at different positions, however, tend to be activated by different spinal segments. Thus the segmental innervation of ganglion cells is correlated with the position rather than the function of post-ganglionic targets. 2. The role of target position in ganglion cell innervation was examined directly by recording from neurones sending axons to different destinations. Superior cervical ganglion cells running dorso-medially in a spinal nerve receive, on average, innervation from more caudal segments than cells projecting ventro-laterally. 3. These selective connexions do not depend on intraganglionic cell position: neurones located at different points along the major axes of the superior cervical ganglion receive, on average, the same segmental innervation. In accord with this observation, retrogradely labelled neurones innervating a particular target such as the eye or ear are widely and randomly distributed within a large portion of the ganglion. Thus the importance of post-ganglionic target position in ganglion cell innervation is not simply a reflexion of ganglionic topography. 4. We conclude that one purpose of the selective connexions in the superior cervical ganglion is to bring together preganglionic axons arising from different levels of the spinal cord and ganglion cells whose axons innervate particular regions of the superior cervical territory.