Presynaptic inhibition of primary afferent transmitter release by 5- hydroxytryptamine at a mechanosensory synapse in the vertebrate spinal cord

Sillar, Keith T.; Simmers, A. J.

doi:10.1523/jneurosci.14-05-02636.1994

Cited by 61 publications

(45 citation statements)

References 32 publications

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“…Both pre-and post-synaptic spinal actions of 5-HT have been demonstrated previously (e.g. Sillar & Simmers, 1994;Hori et al, 1996;Travagli & Williams, 1996;El Manira et al, 1997;Murase et al, 1990;LopezGarcia, 1998). …”

Section: Synaptic Depressionsupporting

confidence: 53%

Pharmacological characterization of serotonin receptor subtypes modulating primary afferent input to deep dorsal horn neurons in the neonatal rat

Garraway

Hochman

2001

British J Pharmacology

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1 Spinal cord slices and whole-cell patch clamp recordings were used to investigate the eects of serotonergic receptor ligands on dorsal root-evoked synaptic responses in deep dorsal horn (DDH) neurons of the neonatal rat at postnatal days (P) 3 ± 6 and P10 ± 14. 2 Bath applied 5-hydroxytryptamine (5-HT) potently depressed synaptic responses in most neurons. Similarly, the 5-HT 1/7 receptor agonist, 5-carboxamidotryptamine (5-CT) depressed synaptic responses. This action was probably mediated by 5-HT 1A receptor activation, since it occurred in the presence of the 5-HT 7 receptor antagonist clozapine and was not observed in the presence of NAN-190, a 5-HT 1A receptor antagonist. In the absence of any agonist, 5-HT 1A receptor antagonists often facilitated synaptic responses, suggesting that there is sucient endogenous 5-HT to tonically activate 5-HT 1A receptors. 3 8-hydroxy-2-(di-n-propylamino) tetralin (8-OH-DPAT), the 5-HT 1A/7 receptor agonist, facilitated synaptic responses, an action probably mediated by 5-HT 7 receptors, since the facilitation could be reversed by subsequent application of the 5-HT 7 receptor antagonist clozapine. 4 Agonists for the 5-HT 1B , 5-HT 2 and 5-HT 3 receptors exerted only modest modulatory actions. 5 A pharmacological analysis of the depression evoked by 5-HT suggested an action partly mediated by 5-HT 1A receptor activation, since antagonism of the 5-HT 1A receptor with NAN-190 or WAY-100635 partly reversed 5-HT-evoked depression. In comparison, 5-HT 7 receptor activation could account for much of the 5-HT-evoked facilitation. 6 We conclude that 5-HT is capable of modulating sensory input onto DDH neurons via several receptor subtypes, producing both facilitatory and depressant actions. Also, the actions of most receptor ligands on the evoked responses were similar within the ®rst 2 postnatal weeks.

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Section: Synaptic Depressionsupporting

confidence: 53%

Pharmacological characterization of serotonin receptor subtypes modulating primary afferent input to deep dorsal horn neurons in the neonatal rat

Garraway

Hochman

2001

British J Pharmacology

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“…Therefore, the reduction of N-and P-type currents could contribute to the previously reported presynaptic inhibition of transmitter release from R-B neurons (Sillar and Simmers, 1994).…”

Section: Modulation Of the T-type Currentsmentioning

confidence: 80%

“…5-HT has been reported previously to mediate presynaptic inhibition of transmitter release from R-B neurons in Xenopus (Sillar and Simmers, 1994). However, T-type channels generally are not thought to be involved in supporting synaptic transmission.…”

Section: Modulation Of the T-type Currentsmentioning

confidence: 98%

“…Previous reports have demonstrated that 5-HT mediates presynaptic inhibition of transmitter release from Xenopus primary sensory neurons: Rohon-Beard (R-B) neurons (Sillar and Simmers, 1994). We therefore examined the effects of 5-HT on voltage-dependent Ca 2ϩ channels in acutely isolated R-B neurons.…”

mentioning

confidence: 96%

“…We found that 5-HT inhibits both the N-, P/Q-type HVA currents and the T-type currents. Although the modulation of HVA currents could contribute to the presynaptic inhibition of transmitter release from R-B neurons (Sillar and Simmers, 1994), the modulation of T-type currents suggests an additional and important locus for modulation of sensory pathways.…”

mentioning

confidence: 99%

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Serotonergic Inhibition of the T-Type and High Voltage-Activated Ca²⁺Currents in the Primary Sensory Neurons ofXenopusLarvae

Sun

Dale

1997

J. Neurosci.

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The primary sensory Rohon-Beard (R-B) neurons of Xenopus larvae are highly analogous to the C fibers of the mammalian pain pathway. We explored the actions of 5-HT by studying the modulation of Ca 2ϩ currents. In ϳ80% of the acutely isolated R-B neurons, 5-HT inhibited the high voltage-activated (HVA) currents by 16% (n ϭ 29) and the T-type currents by 24% (n ϭ 41). The modulation of the T-type and the HVA currents was mimicked by selective 5-HT 1A and 5-HT 1D agonists: 8-OH-DPAT and L-694,247. The effects of the agonists were blocked by their respective 5-HT 1A or 5-HT 1D antagonists: p-MPPI and GR127935, suggesting that both 5-HT 1A and 5-HT 1D receptors were involved. Approximately 70% of the actions of 5-HT on HVA currents was occluded by -conotoxin-GVIA (N-type channel blocker), whereas the rest of the modulation (ϳ30%) was occluded by Ͻ100 nM -agatoxin-TK (P/Q-type channel blocker). This suggests that 5-HT acts on N-and P/Q-type Ca 2ϩ channels. Neither the modulation of the T-type nor that of the HVA currents was accompanied by changes in their voltage-dependent kinetics. Cell-attached patch-clamp recordings suggest that the modulation of the T-type channel occurs through a membrane-delimited second messenger. We have studied the functional consequences of the modulation of T-type Ca 2ϩ channels and have found that these channels play a role in spike initiation in R-B neurons. Modulation of T-type channels by 5-HT therefore could modulate the sensitivity of this sensory pathway by increasing the thresholds of R-B neurons. This is a new and potentially important locus for modulation of sensory pathways in vertebrates.

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Synaptic and nonsynaptic monoaminergic neuron systems in the lamprey spinal cord

et al. 1996

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In the lamprey spinal cord, dopamine- (DA) and 5-hydroxytryptamine-(5-HT) containing cells appear to play an important role in controlling the firing properties of motoneurons and interneurons and, thereby, in modulating the efferent motor pattern. To determine the detailed morphology and synaptic connectivity of the intraspinal DA and 5-HT systems in Lampetra fluviatilis and Ichthyomyzon unicuspis, DA and 5-HT antisera were used in light and electron microscopic immunocytochemical experiments. Two main groups of labeled cells were distinguished: DA-containing liquor-contacting (LC) cells distributed along the central canal, and 5-HT+DA-containing multipolar cells located near the midline ventral to the central canal. Both types were synaptically connected with other neuronal elements. The DA-immunoreactive LC cells, which extended a ciliated process into the central canal, received symmetrical synapses from unlabeled terminals containing small synaptic vesicles. The distal process of the LC cells could be traced to the lateral cell column, to the ventral aspect of the dorsal column, or to the ventromedial area. Ultrastructural analysis of DA fibers in these regions showed the presence of labeled terminals containing numerous small synaptic vesicles and a few dense-core vesicles. These terminals formed symmetrical synapses with unlabeled cell bodies and dendrites, with GABA-immunopositive LC cells, and with the multipolar DA+5-HT cells. The multipolar DA+5-HT cells also received input from unlabeled synapses. Intracellular recording from these cells showed that they received excitatory postsynaptic potentials in response to stimulation of fibers in the ventromedial tracts and dorsal roots. The terminals of the multipolar DA+5-HT neurons in the ventromedial spinal cord contained numerous dense-core vesicles and small synaptic vesicles, but no synaptic specializations could be detected. In addition, a small number of larger DA-immunoreactive cells were observed in the lateral cell column at rostral levels. The lamprey spinal cord thus contains distinct populations of synaptically interconnected monoaminergic neurons. Dopamine-containing LC cells synapse onto DA+5-HT-containing multipolar cells, in addition to GABAergic LC cells and unidentified spinal neurons. In contrast, the multipolar cells appear to exert their influence by nonsynaptic mechanisms.

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Presynaptic inhibition of primary afferent transmitter release by 5- hydroxytryptamine at a mechanosensory synapse in the vertebrate spinal cord

Cited by 61 publications

References 32 publications

Pharmacological characterization of serotonin receptor subtypes modulating primary afferent input to deep dorsal horn neurons in the neonatal rat

Pharmacological characterization of serotonin receptor subtypes modulating primary afferent input to deep dorsal horn neurons in the neonatal rat

Serotonergic Inhibition of the T-Type and High Voltage-Activated Ca²⁺Currents in the Primary Sensory Neurons ofXenopusLarvae

Synaptic and nonsynaptic monoaminergic neuron systems in the lamprey spinal cord

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Presynaptic inhibition of primary afferent transmitter release by 5- hydroxytryptamine at a mechanosensory synapse in the vertebrate spinal cord

Cited by 61 publications

References 32 publications

Pharmacological characterization of serotonin receptor subtypes modulating primary afferent input to deep dorsal horn neurons in the neonatal rat

Pharmacological characterization of serotonin receptor subtypes modulating primary afferent input to deep dorsal horn neurons in the neonatal rat

Serotonergic Inhibition of the T-Type and High Voltage-Activated Ca2+Currents in the Primary Sensory Neurons ofXenopusLarvae

Synaptic and nonsynaptic monoaminergic neuron systems in the lamprey spinal cord

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Serotonergic Inhibition of the T-Type and High Voltage-Activated Ca²⁺Currents in the Primary Sensory Neurons ofXenopusLarvae