Serotonin depolarizes type A and C primary afferents: an intracellular study in bullfrog dorsal root ganglion

Holz, George G.; Shefner, Sarah A.; Anderson, Edmund G.

doi:10.1016/0006-8993(85)91500-8

Cited by 40 publications

(17 citation statements)

References 33 publications

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“…Similar evidence was presented in bullfrog DRG cells in which responses to 5-HT characterized by transient depolarization with membrane conductance increase were frequently observed in C neurons and only exceptionally in A neurons (Holz et al, 1985). In agreement with these studies, our results suggest that 5-HT in p-M concentration induces a fast desensitizing inward current that fulfills the criteria of activation of 5-HT, receptors (Richardson and Engel, 1986;Yakel and Jackson, 1988;Suprenant 1990;Malone et al, 1991).…”

Section: Possible Role Of 5-ht Receptors In Pain Sensationsupporting

confidence: 87%

Serotonin‐ and proton‐induced and modified ionic currents in frog sensory neurons

Philippi

Vyklicky

Kuffler

et al. 1995

J of Neuroscience Research

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Using the whole-cell patch-clamp technique, the effects of serotonin (5-HT) and increased acidity to produce membrane currents and to modify high threshold voltage-dependent calcium currents were studied in isolated dorsal root ganglion (DRG) cells of the frog maintained in short-term culture. DRG cells were classified by morphology into two types: (1) cells with a large number of dark rusty brown granules, and (2) cells devoid of these granules or with few scattered pale granules. Fast application of 5-HT (10-30 microM) induced a rapidly desensitizing inward current with a reversal potential at about 0 mV in 38 of 50 granule-containing neurons (76%) which was never observed (0/35) in "clear" neurons. This current was blocked by 10 nM (+)-tubocurarine. In addition, a small noninactivating outward current was also observed in most DRG neurons during 5-HT superfusion. A sudden decrease of pH from 7.4 to 6 or 5.8 induced a fast inactivating inward current of 100-300 pA in 74% of the "clear" neurons and only 24% of the granule-containing neurons. Small noninactivating membrane currents induced by lowering pH were observed in all neurons. Both 5-HT and increased extracellular H+ reduced the magnitude of high threshold calcium currents in all DRG neurons. It is suggested that the 5-HT receptors are expressed on a morphologically distinct population of neurons while the cells with channels responsible for the fast inactivating proton-induced current cannot be related to any distinct morphological cell type.

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Section: Possible Role Of 5-ht Receptors In Pain Sensationsupporting

confidence: 87%

Serotonin‐ and proton‐induced and modified ionic currents in frog sensory neurons

Philippi

Vyklicky

Kuffler

et al. 1995

J of Neuroscience Research

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“…Similarly an overall membrane hyperpolarization could reduce the probability of the receptor potential reaching spiking threshold. It is well established that 5-HT decreases a Ki current, the S current, in several types of neurons including Aplysia sensory neurons (Klein et al, L982;Pollock and Camardo, 1987) and Bullfrog DRG cells (Holz et al, 1985), resulting in depolarizations of the soma membrane of 5-6 mV. We did not observe significant changes in resting membrane potential.…”

Section: Discussionmentioning

confidence: 68%

Primary afferent responses of a crustacean mechanoreceptor are modulated by proctolin, octopamine, and serotonin

Pasztor

Bush

1989

J. Neurobiol.

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Modulation of sensory responses recorded intracellularly in primary sensory afferents of a crustacean proprioceptor is described. The neuropeptide proctolin enhances the sensory response, whereas the bioamines octopamine and serotonin depress it. The lobster oval organ of the second maxilla, a simple stretch receptor lacking centrifugal control, provides a useful model for studies on nonsynaptic modulation at peripheral sensory loci. Its three large afferents, X, Y, and Z, were prepared for intracellular recording and tested under five experimental conditions: (1) when fully rested, (2) when adapted to maintained stretch and firing tonically, (3) when showing reduced responses after habituation to repetitive stimulation, (4) not stretched but depolarized with current injections, (5) after TTX blockade. The results, taken together, indicate that conductances contributing to the overall amplitude of the receptor potential are major targets for modulators. Thus proctolin increased receptor potential amplitudes with consequent augmentation of spiking, whereas serotonin and octopamine depressed the receptor potentials, often to subthreshold levels with loss of spiking. Octopamine was a less potent agent than serotonin and failed to act upon fibers under TTX blockade. Fibers Y and Z consistently showed sensitivity to the modulators tested. The largest fiber, X, typically was resistant to proctolin, octopamine, and serotonin. Threshold concentrations of 10(-10)-10(-11) M determined in vitro are well below the circulating levels for serotonin and octopamine found in vivo. Proctolin, however, is usually not detectable in the hemolymph, and it is suggested that a significant site of proctolin release may be the oval organ itself.

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“…Very intense hybridization signals were observed within a subset of neurons in dorsal root ganglia. 5-HT3 receptor agonists have been shown to excite peripheral nociceptive terminals (7,43), and presynaptic 5-HT3 receptors on the central terminals of dorsal root ganglion neurons have been observed in the superficial layers of the dorsal horn (42). These results support a role for 5-HT3 receptors in the modulation of activity in primary sensory afferent fibers.…”

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confidence: 60%

Nervous system distribution of the serotonin 5-HT3 receptor mRNA.

Tecott

Maricq

Julius

1993

Proc. Natl. Acad. Sci. U.S.A.

321

177

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The serotonin 5-HT3 receptor subtype has been implicated in many brain functions. Antagonists of this receptor have anxiolytic and antiemetic effects in humans and in animal models. To determine with cellular resolution the distribution of 5-HT3 receptor mRNA, in situ hybridization was performed in sections of mouse brain and dorsal root ganglia. Scattered labeled cells were observed throughout cortical regions, with highest densities in the piriform, cingulate, and entorhinal areas. Strong hybridization signals were seen in the hippocampal formation, where expression appeared primarily in interneurons. Labeled cells were most abundant in the posteroventral hippocampal region, particularly in the lacunosum moleculare layer of CAL. This distribution suggests that 5-HT3 receptors may mediate the known serotonergic inhibition of pyramidal cell populations via excitation of inhibitory interneurons. Labeled cells were also observed in the major subdivisions of the amygdaloid complex, the olfactory bulb, the trochlear nerve nucleus, the dorsal tegmental region, the facial nerve nucleus, the nucleus of the spinal tract of the trigeminal nerve, and the spinal cord dorsal horn. In the periphery, intense hybridization signals were seen in a subpopulation of cells in dorsal root ganglia. The data correlate generally with physiological, behavioral, and receptor autoradiographic studies, provide cellular resolution, and reveal regions of receptor expression not previously observed. The distribution of 5-HT3 receptor mRNA is consistent with roles for the receptor in cognition and affect and in the modulation of sensory input.The monoamine serotonin (5-hydroxytryptamine) has been implicated in a variety of central and peripheral nervous system processes. Its diverse effects are mediated by subclasses of serotonin receptors that were initially defined on the basis of distinct ligand binding profiles (1). Biochemical and molecular genetic characterization of these receptors demonstrates that the 5-HT1, 5-HT2, and 5-HT4 receptor subclasses belong to the superfamily of guanine nucleotide binding protein-coupled receptors (2, 3). In contrast, serotonin 5-HT3 receptors are ligand-gated ion channels that mediate fast excitatory responses (4-6).Responses mediated by 5-HT3 receptors have been characterized in the peripheral nervous system, suggesting roles for the receptor in nociception and gut motility (7)(8)(9)(10). Recently, 5-HT3 receptors have been observed in the brain and have been implicated in many central nervous system processes (11, 12). High levels of 5-HT3 radioligand binding have been detected in the area postrema and solitary tract nucleus (13,14). The antiemetic effects of 5-HT3 antagonists may be attributed to actions at these sites (15,16). Receptor autoradiographic studies have also demonstrated localization of 5-HT3 receptors to cortical and limbic system regions (14,17,18). 5-HT3 receptor antagonists have anxiolytic effects in humans and in animal models (12, 19), perhaps through action at these sites. Re...

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Serotonin depolarizes type A and C primary afferents: an intracellular study in bullfrog dorsal root ganglion

Cited by 40 publications

References 33 publications

Serotonin‐ and proton‐induced and modified ionic currents in frog sensory neurons

Serotonin‐ and proton‐induced and modified ionic currents in frog sensory neurons

Primary afferent responses of a crustacean mechanoreceptor are modulated by proctolin, octopamine, and serotonin

Nervous system distribution of the serotonin 5-HT3 receptor mRNA.

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