Synaptic Vesicle Depletion in Reticulospinal Axons is Reduced by 5‐hydroxytryptamine

Direct Evidence for Presynaptic Modulation of Glutamatergic Transmission

O. Shupliakov, V. A. Pieribone, H. Gad, L. Brodin

Research outputpeer-review

33 Citations (Scopus)

Abstract

5‐hydroxytryptamine (5‐HT; serotonin) is known to depress glutamatergic synaptic transmission in the spinal cord of vertebrates. To test directly whether 5‐HT inhibits synaptic glutamate release, we examined its effect on the ultrastructure of synaptic vesicle clusters in giant reticulospinal axons in a lower vertebrate (lamprey; Lampetra fluviatilis). The size of these axons makes it possible to selectively expose only a part of the presynaptic element to 5‐HT, while another part of the same axon is maintained in control solution. Action potential stimulation at 20 Hz for 20 min caused a marked reduction in the number of synaptic vesicles in active zones maintained in control solution, while in the part exposed to 5‐HT (20 μM) the number of synaptic vesicles per active zone was ‐3‐fold higher. In contrast, 5‐HT had no effect on the number of vesicles in resting axons. To examine whether 5‐HT acts by reducing presynaptic Ca2+ influx, intra‐axonal recordings of Ba2+ potentials were performed. No reduction of the axonal Ba2+ potential could be detected after application of 20 or 200 pM 5‐HT. The present results show that 5‐HT reduces the rate of synaptic exocytosis in reticulospinal axons. The effect appears to be mediated by a mechanism distinct from the presynaptic Ca2+ channels.

Original languageEnglish
Pages (from-to)1111-1116
Number of pages6
JournalEuropean Journal of Neuroscience
Volume7
Issue number5
DOIs
Publication statusPublished - 1 Jan 1995

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Synaptic Vesicles
Axons
Vertebrates
Lampreys
Exocytosis
Synaptic Transmission
Action Potentials
Glutamic Acid
Serotonin
Spinal Cord

Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Synaptic Vesicle Depletion in Reticulospinal Axons is Reduced by 5‐hydroxytryptamine: Direct Evidence for Presynaptic Modulation of Glutamatergic Transmission",
abstract = "5‐hydroxytryptamine (5‐HT; serotonin) is known to depress glutamatergic synaptic transmission in the spinal cord of vertebrates. To test directly whether 5‐HT inhibits synaptic glutamate release, we examined its effect on the ultrastructure of synaptic vesicle clusters in giant reticulospinal axons in a lower vertebrate (lamprey; Lampetra fluviatilis). The size of these axons makes it possible to selectively expose only a part of the presynaptic element to 5‐HT, while another part of the same axon is maintained in control solution. Action potential stimulation at 20 Hz for 20 min caused a marked reduction in the number of synaptic vesicles in active zones maintained in control solution, while in the part exposed to 5‐HT (20 μM) the number of synaptic vesicles per active zone was ‐3‐fold higher. In contrast, 5‐HT had no effect on the number of vesicles in resting axons. To examine whether 5‐HT acts by reducing presynaptic Ca2+ influx, intra‐axonal recordings of Ba2+ potentials were performed. No reduction of the axonal Ba2+ potential could be detected after application of 20 or 200 pM 5‐HT. The present results show that 5‐HT reduces the rate of synaptic exocytosis in reticulospinal axons. The effect appears to be mediated by a mechanism distinct from the presynaptic Ca2+ channels.",
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T2 - Direct Evidence for Presynaptic Modulation of Glutamatergic Transmission

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AU - Pieribone, V. A.

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AU - Brodin, L.

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N2 - 5‐hydroxytryptamine (5‐HT; serotonin) is known to depress glutamatergic synaptic transmission in the spinal cord of vertebrates. To test directly whether 5‐HT inhibits synaptic glutamate release, we examined its effect on the ultrastructure of synaptic vesicle clusters in giant reticulospinal axons in a lower vertebrate (lamprey; Lampetra fluviatilis). The size of these axons makes it possible to selectively expose only a part of the presynaptic element to 5‐HT, while another part of the same axon is maintained in control solution. Action potential stimulation at 20 Hz for 20 min caused a marked reduction in the number of synaptic vesicles in active zones maintained in control solution, while in the part exposed to 5‐HT (20 μM) the number of synaptic vesicles per active zone was ‐3‐fold higher. In contrast, 5‐HT had no effect on the number of vesicles in resting axons. To examine whether 5‐HT acts by reducing presynaptic Ca2+ influx, intra‐axonal recordings of Ba2+ potentials were performed. No reduction of the axonal Ba2+ potential could be detected after application of 20 or 200 pM 5‐HT. The present results show that 5‐HT reduces the rate of synaptic exocytosis in reticulospinal axons. The effect appears to be mediated by a mechanism distinct from the presynaptic Ca2+ channels.

AB - 5‐hydroxytryptamine (5‐HT; serotonin) is known to depress glutamatergic synaptic transmission in the spinal cord of vertebrates. To test directly whether 5‐HT inhibits synaptic glutamate release, we examined its effect on the ultrastructure of synaptic vesicle clusters in giant reticulospinal axons in a lower vertebrate (lamprey; Lampetra fluviatilis). The size of these axons makes it possible to selectively expose only a part of the presynaptic element to 5‐HT, while another part of the same axon is maintained in control solution. Action potential stimulation at 20 Hz for 20 min caused a marked reduction in the number of synaptic vesicles in active zones maintained in control solution, while in the part exposed to 5‐HT (20 μM) the number of synaptic vesicles per active zone was ‐3‐fold higher. In contrast, 5‐HT had no effect on the number of vesicles in resting axons. To examine whether 5‐HT acts by reducing presynaptic Ca2+ influx, intra‐axonal recordings of Ba2+ potentials were performed. No reduction of the axonal Ba2+ potential could be detected after application of 20 or 200 pM 5‐HT. The present results show that 5‐HT reduces the rate of synaptic exocytosis in reticulospinal axons. The effect appears to be mediated by a mechanism distinct from the presynaptic Ca2+ channels.

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