Quantitative in vitro studies on the nerve growth factor (NGF) requirement of neurons. II. Sensory neurons.
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Evidence for new catecholamines or related amino acids in some invertebrate sensory neurons.
In certain sensory neurons of many different invertebrate species, including the sea anemones. Metridium senile and Tealia felina and the crustacean Artemia salina, fluorophores are formed during the course of the fluorescent histochemical technique of Falck-Hillarp. The presumed catecholamine nature of the neuronal fluorogenic compound was investigated by microspectrofluorometry, and the spectral characteristics of the fluorescence in the taxonomically different species was found to be very similar (excitation maximum at 375 nm with a smaller peak or shoulder at 330 nm and sometimes a shoulder in the spectrum at 410 nm; emission maximum at 475 nm). The emission maximum coincides with that of the catecholamines and DOPA (475 nm). The excitation maximum (375 nm) directly after formaldehyde treatment, however- differs from that of the catecholamines and DOPA (410 nm), but is similar to the excitation maximum displayed by these catechol derivatives at acid pH. The spectral characteristics of the fluorophore in the sensory cells might therefore theoretically be explained by an acid pH in the cells. This means improbable, however, and it is suggested that the phenomenon is due to the presence of unknown catechol derivatives. Analyses of the pH-dependent spectral changes indicate that the presumed catechol derivative in Tealia felina is beta-hydroxylated, whereas that in Artemia salina is not.
Amino Acids↗
Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons.
The neurogenetic process leading to the formation of primary sensory neurons persists into adult life in the olfactory epithelium of mammals. The morphological stages of maturation and ageing of this exceptional neuron have been described both at light and electron microscopical levels. For descriptive purposes the neural elements have been classified as: (1) basal cells proper, (2) globose basal cells, and (3) neurons. Intermediate stages, however, have been identified. Autoradiographic observations complement the morphological studies and provide a time sequence of the morphological stages leading to the mature neurons. A typical columnar arrangement of the sensory neurons has been described. Furthermore, active and quiescent zones have been recognized in the neuroepithelium. In the active zones the neurogenetic process is vigorous, and the zones are characterized by the presence of immature elements. However, in the quiescent zones there exists a population of mature elements while immature neurons are sparse.
Animals↗
Nucleolin promotes neuropathic pain by increasing chromatin accessibility at the Ccl2 promoter in primary sensory neurons.
Nerve injury-induced transcriptional alterations in primary sensory neurons of the dorsal root ganglion (DRG) constitute a key molecular basis for the development of neuropathic pain. Nucleolin (NCL), a highly conserved multifunctional nucleolar protein, regulates gene transcription. Here, we identify that NCL is expressed exclusively in the nuclei of DRG neurons. Peripheral nerve injury time-dependently upregulates Ncl mRNA and NCL protein levels in injured DRG neurons. Blocking this upregulation through DRG microinjection of the adeno-associated virus 9 (AAV9) expressing an shRNA targeting Ncl attenuates nerve injury-induced increases of C-C motif chemokine ligand 2 (CCL2) mRNA and its protein in injured DRG and alleviates the development and maintenance of mechanical, heat and cold hypersensitivities. Conversely, mimicking DRG NCL upregulation through DRG microinjection of AAV9 carrying the full-length Ncl coding sequence increases Ccl2 mRNA and CCL2 protein levels in microinjected DRGs and produces neuropathic pain-like symptoms in the absence of nerve injury. Mechanistically, peripheral nerve injury increases NCL occupancy at the Ccl2 promoter and enhances chromatin accessibility at this locus, resulting in elevated CCL2 expression in injured DRG neurons, which is reversed by NCL knockdown. Given that Ncl mRNA is co-expressed with Ccl2 mRNA in individual DRG neurons, our findings suggest that NCL upregulation in the DRG contributes to neuropathic pain likely by increasing chromatin accessibility at the Ccl2 promoter in primary sensory neurons.
Animals↗
Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex in Aplysia.
We have identified the processes of mechanoreceptor sensory neurons by intracellular injection of horseradish peroxidase in order to study the structure of synapses which exhibit profound, behaviourally-relevant plasticity. These synapses are located at small, varicose expansions along or at the end of the fine, microtubule-containing neurites, and they are crowded with vesicles some of which are associated with the varicosity membrane at regions of membrane specialization morphologically equivalent to active zones described in other species. These active zones occur between pre- and postsynaptic processes at two varieties of apposition: a conventional flat one, and a more elaborate indented one. At indented appositions, the presynaptic varicosity is invaginated by a thin (less than 0.25 micrometer diameter) spine of variable length. The active zones of indented synapses have approximately twice the vesicle frequency of flat synapses, suggesting that indented synapses are more effective. Sensory neuron terminals are relatively uniform in their structure, having similar concentrations of vesicles and numbers of active zones, and the majority of the processes postsynaptic to them are less than 0.5 micrometer in diameter. These regularities, and the presence of two strikingly-different types of synaptic apposition, flat and indented, should facilitate structural comparisons of neurons from naive and behaviourally-modified animals. The possible dynamic interconversion of indented and flat appositions at the synaptic terminals of sensory neurons and its behavioural relevance are discussed.
Animals↗
Deep FLASH-seq profiling of purified canine sensory neurons uncovers species-specific signatures relevant to pain and itch.
Naturally occurring pain and itch disorders in the domestic dog represent an important and underexploited opportunity for translational sensory neuroscience. These conditions largely mirror human disease, highlighting the need for detailed comparative understanding of canine somatosensory neurobiology. Here, we present a single-cell transcriptomic characterisation of the canine dorsal root ganglion (DRG), providing molecular insights into sensory neuron diversity in a species of direct veterinary and biomedical relevance. We develop a novel mechanical dissociation and fluorescence-activated cell sorting strategy enabling purification of intact whole neurons from adult canine DRG, followed by deep, full-length RNA sequencing using FLASH-seq. This approach yields high-quality transcriptional profiles with molecular depth analogous to deep neuronal profiling in human DRG, enabling resolution of neuronal identities and subtype-specific gene programs. Using these data, we identify canine sensory neuron clusters conforming to conserved principles of DRG molecular organization observed across species, including peptidergic and noncanonical peptidergic nociceptors, low-threshold mechanoreceptors, proprioceptors, and thermosensory populations. Cross-species comparisons with human and mouse DRG datasets reveal broad conservation of pain- and itch-relevant pathways and therapeutic targets, alongside biologically meaningful divergence. We further identify species-specific differences in subtype-restricted expression of the pharmacologically relevant receptors IL31RA and SSTR2 , which we validate using in situ hybridization and contextualize with human spatial transcriptomic data. Finally, we provide evidence that domestication-associated genes are nonrandomly enriched in specific sensory neurons, suggesting that evolutionary history may have shaped somatosensory function. These data represent a resource for comparative sensory neuroscience and inform translational interpretation of pain and itch therapeutics across species.
Animals↗
[Comparative morphometric study of sensory neurons of the cerebral and spinal cord ganglia following transection of their processes].
The morphometrical study of sensory neurons g. nodosum of the vagus nerve and spinal ganglia after transection of central and peripheral processes has established similar reactions of the neurons of these ganglia. The sensory neurons respond to the transection of peripheral processes by phenomena of retrograde degeneration. No retrograde degeneration was observed in the neurons after transection of central processes. The diminution of the size of the nerve cell bodies, their nuclei and nucleoli was noted at the period of maximally pronounced phenomena of retrograde degeneration as well as fragmentation and peripheral displacement of the Golgi apparatus, increased amount of satellites adjacent to retrogradely changed neurons.
Animals↗
Contribution of individual mechanoreceptor sensory neurons to defensive gill-withdrawal reflex in Aplysia.
1. To evaluate the contribution which mechanoreceptor sensory neurons make to the defensive gill-withdrawal reflex we developed an isolated reflex preparation. We then reduced this isolated reflex to a microcircuit (consisting of a single sensory cell and single motor cell) so as to causally relate the contribution of individual cells to the expression and plastic properties of the behavior. 2. Mechanoreceptor neurons make significant contributions to the amplitude and duration of the complex PSP in the motor neurons. A single spike in a sensory neuron produces an EPSP in the motor neuron which accounts for 7-36% of the complex EPSP produced by weak tactile stimulation of the skin. 3. More than 50% of the synaptic input to the gill motor neurons appears to be monosynaptic. Perfusing the ganglion with solutions of high divalent cations reduced the motor neurons' complex PSP by only 40%. 4. The population response of the mechanoreceptors to a point stimulus can be simulated by repetitively firing a single sensory neuron. Firing a single sensory cell discharges the motor neuron and produces a gill contraction similar to that produced by a natural stimulus. 5. Mechanoreceptors make monosynaptic connections onto gill motor neurons which decrement with repeated stimulation paralleling the decrement of the complex PSP to punctate tactile stimulation of the skin. 6. The results indicate that the known neural elements may quantitatively account for most of the expression of the behavior and its short-term habituation.
Animals↗
Specificity of retrograde transport of nerve growth factor (NGF) in sensory neurons: a biochemical and morphological study.
In previous studies it has been shown that nerve growth factor (NGF) is taken up with a high selectivity by adrenergic nerve terminals and is transported retrogradely to the perikaryon11,22. It was the aim of the present experiments to investigate whether the sensory neurons exhibit the same high degree of selectivity for retrograde transport throughout the whole life cycle, although it is known that their dramatic response to NGF is confined to a short period of ontogenetic development. Unilateral injection of [125I]NGF into the forepaw of adult rats was followed by a preferential accumulation of radioactivity in the sensory ganglia (C6-C7) of the injected side. However, this preferential accumulation was not detectable earlier than 6 h after injection and reached a maximum (ratio between injected and non-injected side, 5:1) after 11-16 h. Transection of the plexus brachialis abolished and local administration of colchicine prior to that of [125I]NGF greatly reduced the preferential accumulation of radioactivity in the ganglia of the injected side. The rate of retrograde transport of NGF in sensory neurons was calculated to be 13 mm/h which is about 5 times faster than that in adrenergic neurons. The selectivity of this retrograde transport was demonstrated by the fact that injection of 125I-labeled bovine serum albumin and cytochrome c did not result in a preferential accumulation of radioactivity in the sensory ganglia of the injected side. Light microscopic autoradiography revealed heavily labeled cells in the sensory ganglia (C6-C7) of the injected side after administration of [125I]NGF into the forepaw. Only cells belonging to the large cell type were labeled. Prolonged (7 mug/g/day over 5 days) injection of NGF into the forepaw of 10-day-old rats did not result in a hypertropic response of the sensory neurons as far as can be judged from morphometric studies at the light microscopic level.
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Membrane properties and conduction velocity in sensory neurones following central or peripheral axotomy.
1. The properties of dorsal root ganglion cells in the lumbosacral segments were examined with intracellular electrodes about 3 weeks after section of the central (dorsal roots) or peripheral processes in the cat.2. Chronic section of the peripheral nerve in the hind limb resulted in a reduction in conduction velocity of both the central and peripheral processes of sensory neurones.3. Sensory neurones arising from the triceps surae and plantaris muscles were subject to ;disuse' conditions for about 3 weeks by section of the ventral roots combined with severance of the Achilles tendon. Under such conditions, the central and peripheral conduction velocities of these sensory neurones tended to decrease, but the decrease was significantly less than that following peripheral nerve section.4. Chronic section of the dorsal roots produced no significant changes in conduction velocity of the central processes of muscle sensory neurones but caused a significant increase in the peripheral conduction velocity.5. The only electrophysiological property of dorsal root ganglion cells which altered following axotomy was the time-dependent membrane rectification in response to hyperpolarizing current pulses. The rectification characteristics were modified by chronic section of the peripheral nerve but not by chronic section of the dorsal root.6. It is concluded that injuries in nerve fibres per se do not necessarily result in a decrease of their conduction velocity and that a decrease in their conduction velocity is associated with changes in the properties of the cell bodies.7. It is suggested that a decrease in conduction velocity following nerve section may require the participation of changes in the neurone cell body.
Animals↗
Appearance of histochemically detectable ionic calcium in degenerating primary sensory neurons.
The effect of neonatal capsaicin treatment on the fine structure and localization of ionic calcium in sensory ganglion cells has been investigated in rats. Neonatal capsaicin treatment resulted in the degeneration of certain type B sensory neurons. At the same time ionic calcium was demonstrated histochemically in the perikarya of numerous small-sized ganglion cells. The appearance of histochemically detectable ionic calcium in these cells in relation to the pharmacologically evoked degeneration of certain primary sensory neurons is discussed.
Animals↗
Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy.
This report describes the retrograde degeneration affecting olfactory sensory neurons of rats after severance of their axons and illustrates the reconstitution of new neurons originating from stem cells located at the base of the olfactory neuroepithelium. Degeneration of the mature, axotomized neurons, signalled by an increased electron density of their cytoplasmic matrix and by the appearance of lipofuscin-like granules, can be detected in the neuroepithelium as early as 24 h after surgery and becomes conspicuous between the second and the third day. Degenerating neurons can be observed in decreasing number up to the tenth post-operative day. They are removed by macrophages which invade the epithelium. The reconstitution of new neurons begins to occur after eight days, when the stem cells undergo vigorous mitotic activity and differentiate into neurons. The morphology of the reconstituted neurons has been described in detail at different stages of their maturation. After 30 days, the olfactory epithelium appears similar to controls. On the basis of both morphological (in rats) and autoradiographic ( in mice) observations, the basal cells have been recognized as stem cells of the olfactory neurons.
Animals↗
[Long-term transplantation of mature sensory neurons].
The spinal ganglia were transplanted into the mesocolon of adult cats for periods of from 1 day to 9 months. About 30% of differentiated sensory neurons survived during the longterm transplantation. The intensive regeneration of the sensory neurons processes was characteristic of the transplanted neurons. Total myelinization of the regenerating nerves occurred during the 3rd--5th month. Potential regeneration capacity of the differentiated neurons and possibly of their prolonged transplantation were revealed.
Animals↗
Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration.
Sensory neurons grown in dispersed cell culture in the absence of non-neuronal cell types contain immunoreactive substance P that is chemically similar to synthetic substance P. When depolarized in high-K+ media (30-120 mM), the neurons release this peptide by a Ca2+-dependent mechanism. An enkephalin analogue, [D-Ala2]enkephalin amide, at 10 micron inhibits the K+-evoked release of substance P. At the same or lower concentrations, [D-Ala2]enkephalin amide and enkephalin decrease the duration of the Ca2+ action potential evoked and recorded in dorsal root ganglion cell bodies without affecting the resting membrane potential or resting membrane conductance. This modulation of voltage-sensitive channels may account for the inhibition of substance P release.
Action Potentials↗
Further observations on transganglionic degeneration in trigeminal primary sensory neurons.
Transganglionic degeneration has been studied with the Fink-Heimer method in the trigeminal sensory nuclei of adult cats and rats following peripheral nerve transections. Degeneration was observed ipsilaterally as well as contralaterally in all cats, surviving 11-30 days after transection of the infraorbital nerve. In the rats the infraorbital or the auriculotemporal nerve was transected. After transection of the former nerve the first signs of transganglionic degeneration were observed after 7 days postoperative survival and even after 130 days there were still a lot of degenerating structures present. Between 7 and 14 days survival there was a small amount of degeneration in substantia gelatinosa. After transection of the auriculotemporal nerve, degeneration was observed only in the most caudal parts of the trigeminal sensory nuclear complex. Opposite to the situation in the cat, there was no contralateral degeneration in the rat. All degeneration areas were somatotopically organized, both in the cat and in the rat. The results are discussed in relation to a previous study of transganglionic degeneration in the trigeminal sensory nuclear complex by the authors and to anatomical and physiological studies of somatotopic organization in the trigeminal sensory nuclei. They clearly show the value of transganglionic degeneration used as a tool for analysis of central projections of primary sensory neurons.
Age Factors↗
Growth cone formation in cultures of sensory neurons.
Three experimental situations have been found in which cultured sensory neurons from embryonic chicken will form growth cones from positions along the length of the neurite. If the neurons are dissected with a remaining short axonal stump and plated into serum-free medium, they can form a morphologically normal growth cone from the stump within 15 min, even in the presence of cycloheximide or puromycin. When neurites growing in culture media with low levels of serum are cut at any point with microneedles, growth cones are produced quickly from the amputated stump, usually within 20 min. Treatment of growing neurons with low concentrations of colchicine, Colcemid, or podophyllotoxin results in the progressive appearance of lateral filopodia and regions of flattened cytoplasm that closely resemble growth cones except for their preterminal positions. These observations show that the potential to form growth cones is distributed throughout the neuron and suggest that this normally repressed in some way by the neuronal microtubules.
Axons↗
Substance P: depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons.
The substance P content, glutamic acid decarboxylase and choline acetyltransferase activities and the level of [3H]diprenorphine binding were measured in various regions of the lumbar spinal cord of rats after unilateral section of the sciatic nerve or after dorsal rhizotomy. Sciatic nerve section produced a 75--80% depletion of substance P in the dorsal horn but did not change the substance P content of the ventral horn. The onset of substance P depletion occurred within 7 days and was maintained for 2 months. The substance P content of the dorsal root ganglia and both the peripheral and central branches of primary sensory neurons was also reduced after sciatic nerve section. Glutamic acid decarboxylase and choline acetyltransferase activity were unchanged; however, a small decrease in opiate receptor binding occurred 1 month after nerve section. Dorsal rhizotomy produced an 80% depletion of substance P in the dorsal horn. In addition, the substance P content of the ventral horn was significantly reduced. Glutamic acid decarboxylase activity in the dorsal horn was unaffected by dorsal rhizotomy whereas opiate receptor binding was reduced by 40%. From these studies it appears that peripheral nerve injury results in the degeneration of primary sensory neurons which contain and release substance P as neurotransmitter.
Afferent Pathways↗
Sensory neurons in leech central nervous system: changes in potassium conductance an excitation threshold.
1. The sensory neurons in the leech central nervous system differ in their accommodation to linearly rising currents. Advantage was taken of these differences to study the ionic mechanism of accommodation in single pairs of N (noxious), P (pressure), and T (touch) cells. 2. Nonlinearities in membrane-potential changes and current-voltage relationships with square-wave and ramp currents are more pronounced in P and T cells than in N cells. The accommodation coefficients increase in conditions that reflect this delayed rectification. When rectification is absent, the accommodation coefficients depart from unity only slightly or not at all. 3. Accommodation coefficients remain unchanged when half of the chloride in the bathing medium is replaced by sulfate. Accommodation coefficients become greater when the extracellular potassium concentration is reduced from 4 to 0 mM, and decrease when the concentration is raised to 8 mM. The membrane potential changes by only a few millivolts. 4. As extracellular potassium concentration is increased, the action potential is lengthened and the maximal rate of fall of the action potential is reduced. With concentrations greater than 4 mM these relationships are linear, but depart from linearity at lower concentrations. The amplitude of the undershoot decreases linearly as the extracellular potassium concentration increases from 4 to 16 mM, and increases non-linearly at concentrations below 4 mM. 5. The rapid accommodation of leech neurons is based primarily on an increased potassium conductance. The possibility is considered that concentration changes like those produced experimentally may occur naturally, affecting integrative processes in the central nervous system.
Action Potentials↗