Abstract
Glutamate uptake by high-affinity transporters is responsible for limiting the activation of postsynaptic receptors and maintaining low levels of ambient glutamate. The reuptake process generates membrane currents, which can be activated by synaptically released glutamate in glial cells and some postsynaptic neurons. However, less is known about presynaptic transporter currents because the small size of synaptic boutons precludes direct recordings. Here, we have recorded from two giant nerve terminals: bipolar cell synaptic terminals in goldfish retina and the calyx of Held in rat auditory brainstem. Exocytosis was evoked by brief depolarizations and measured as an increase in membrane capacitance. In isolated bipolar cell terminals, exocytosis was associated with an anion (NO3 - or Cl-) current. The current peaked 2.8 msec after the start of the depolarization and decayed with a mean time constant of 8.5 msec. It was inhibited by the nontransportable glutamate transporter antagonist DL-threo-β-benzyloxyaspartate (TBOA) but was insensitive to the GLT1/EAAT2 subtype-selective antagonist dihydrokainate and was affected by extracellular pH buffering. A TBOA-sensitive anion current was also evoked by application of exogenous glutamate to bipolar cell terminals. The large single-channel conductance, derived from noise analysis, and previous immunolocalization studies suggest that synaptically released glutamate activates EAAT5-type transporters in bipolar cell terminals. In contrast, neither exocytosis nor exogenous glutamate evoked a transporter current in the calyx of Held. Glutamate transporter currents with rapid kinetics are therefore identified and characterized in bipolar cell terminals, providing a valuable system for investigating the function and modulation of presynaptic glutamate transporters.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 4831-4841 |
| Number of pages | 11 |
| Journal | Journal of Neuroscience |
| Volume | 23 |
| Issue number | 12 |
| State | Published - Jun 15 2003 |
Fingerprint
Keywords
- Auditory brainstem
- Calyx of Held
- EAAT5 anion current
- Exocytosis
- Glutamate transporters
- Presynaptic terminal
- Retinal bipolar cell
- Synaptic ribbons
- Uptake
ASJC Scopus subject areas
- Neuroscience(all)
Cite this
Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. / Palmer, Mary J.; Taschenberger, Holger; Hull, Court; Tremere, Liisa; Von Gersdorff, Henrique.
In: Journal of Neuroscience, Vol. 23, No. 12, 15.06.2003, p. 4831-4841.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Synaptic activation of presynaptic glutamate transporter currents in nerve terminals
AU - Palmer, Mary J.
AU - Taschenberger, Holger
AU - Hull, Court
AU - Tremere, Liisa
AU - Von Gersdorff, Henrique
PY - 2003/6/15
Y1 - 2003/6/15
N2 - Glutamate uptake by high-affinity transporters is responsible for limiting the activation of postsynaptic receptors and maintaining low levels of ambient glutamate. The reuptake process generates membrane currents, which can be activated by synaptically released glutamate in glial cells and some postsynaptic neurons. However, less is known about presynaptic transporter currents because the small size of synaptic boutons precludes direct recordings. Here, we have recorded from two giant nerve terminals: bipolar cell synaptic terminals in goldfish retina and the calyx of Held in rat auditory brainstem. Exocytosis was evoked by brief depolarizations and measured as an increase in membrane capacitance. In isolated bipolar cell terminals, exocytosis was associated with an anion (NO3 - or Cl-) current. The current peaked 2.8 msec after the start of the depolarization and decayed with a mean time constant of 8.5 msec. It was inhibited by the nontransportable glutamate transporter antagonist DL-threo-β-benzyloxyaspartate (TBOA) but was insensitive to the GLT1/EAAT2 subtype-selective antagonist dihydrokainate and was affected by extracellular pH buffering. A TBOA-sensitive anion current was also evoked by application of exogenous glutamate to bipolar cell terminals. The large single-channel conductance, derived from noise analysis, and previous immunolocalization studies suggest that synaptically released glutamate activates EAAT5-type transporters in bipolar cell terminals. In contrast, neither exocytosis nor exogenous glutamate evoked a transporter current in the calyx of Held. Glutamate transporter currents with rapid kinetics are therefore identified and characterized in bipolar cell terminals, providing a valuable system for investigating the function and modulation of presynaptic glutamate transporters.
AB - Glutamate uptake by high-affinity transporters is responsible for limiting the activation of postsynaptic receptors and maintaining low levels of ambient glutamate. The reuptake process generates membrane currents, which can be activated by synaptically released glutamate in glial cells and some postsynaptic neurons. However, less is known about presynaptic transporter currents because the small size of synaptic boutons precludes direct recordings. Here, we have recorded from two giant nerve terminals: bipolar cell synaptic terminals in goldfish retina and the calyx of Held in rat auditory brainstem. Exocytosis was evoked by brief depolarizations and measured as an increase in membrane capacitance. In isolated bipolar cell terminals, exocytosis was associated with an anion (NO3 - or Cl-) current. The current peaked 2.8 msec after the start of the depolarization and decayed with a mean time constant of 8.5 msec. It was inhibited by the nontransportable glutamate transporter antagonist DL-threo-β-benzyloxyaspartate (TBOA) but was insensitive to the GLT1/EAAT2 subtype-selective antagonist dihydrokainate and was affected by extracellular pH buffering. A TBOA-sensitive anion current was also evoked by application of exogenous glutamate to bipolar cell terminals. The large single-channel conductance, derived from noise analysis, and previous immunolocalization studies suggest that synaptically released glutamate activates EAAT5-type transporters in bipolar cell terminals. In contrast, neither exocytosis nor exogenous glutamate evoked a transporter current in the calyx of Held. Glutamate transporter currents with rapid kinetics are therefore identified and characterized in bipolar cell terminals, providing a valuable system for investigating the function and modulation of presynaptic glutamate transporters.
KW - Auditory brainstem
KW - Calyx of Held
KW - EAAT5 anion current
KW - Exocytosis
KW - Glutamate transporters
KW - Presynaptic terminal
KW - Retinal bipolar cell
KW - Synaptic ribbons
KW - Uptake
UR - http://www.scopus.com/inward/record.url?scp=0037741030&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=0037741030&partnerID=8YFLogxK
M3 - Article
VL - 23
SP - 4831
EP - 4841
JO - Journal of Neuroscience
JF - Journal of Neuroscience
SN - 0270-6474
IS - 12
ER -