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The nature of surround-induced depolarizing responses in goldfish cones.

Kraaij DA, Spekreijse H, Kamermans M - J. Gen. Physiol. (2000)

Bottom Line: It was found that niflumic acid blocks the feedback-induced depolarizing responses in cones, while the shift of the calcium current activation function and the depolarizing biphasic horizontal cell responses remain intact.Polarization of the presynaptic (horizontal) cell leads to calcium influx in the postsynaptic cell (cone), but due to the combined activity of the calcium current and the calcium-dependent chloride current, the membrane potential of the postsynaptic cell will be hardly modulated, whereas the output of the postsynaptic cell will be strongly modulated.Since no polarization of the postsynaptic cell is needed for these feedback-mediated responses, this mechanism of synaptic transmission can modulate the neurotransmitter release in single synaptic terminals without affecting the membrane potential of the entire cell.

View Article: PubMed Central - PubMed

Affiliation: Graduate School Neurosciences Amsterdam, The Netherlands Ophthalmic Research Institute, 1105 BA Amsterdam, The Netherlands.

ABSTRACT
Cones in the vertebrate retina project to horizontal and bipolar cells and the horizontal cells feedback negatively to cones. This organization forms the basis for the center/surround organization of the bipolar cells, a fundamental step in the visual signal processing. Although the surround responses of bipolar cells have been recorded on many occasions, surprisingly, the underlying surround-induced responses in cones are not easily detected. In this paper, the nature of the surround-induced responses in cones is studied. Horizontal cells feed back to cones by shifting the activation function of the calcium current in cones to more negative potentials. This shift increases the calcium influx, which increases the neurotransmitter release of the cone. In this paper, we will show that under certain conditions, in addition to this increase of neurotransmitter release, a calcium-dependent chloride current will be activated, which polarizes the cone membrane potential. The question is, whether the modulation of the calcium current or the polarization of the cone membrane potential is the major determinant for feedback-mediated responses in second-order neurons. Depolarizing light responses of biphasic horizontal cells are generated by feedback from monophasic horizontal cells to cones. It was found that niflumic acid blocks the feedback-induced depolarizing responses in cones, while the shift of the calcium current activation function and the depolarizing biphasic horizontal cell responses remain intact. This shows that horizontal cells can feed back to cones, without inducing major changes in the cone membrane potential. This makes the feedback synapse from horizontal cells to cones a unique synapse. Polarization of the presynaptic (horizontal) cell leads to calcium influx in the postsynaptic cell (cone), but due to the combined activity of the calcium current and the calcium-dependent chloride current, the membrane potential of the postsynaptic cell will be hardly modulated, whereas the output of the postsynaptic cell will be strongly modulated. Since no polarization of the postsynaptic cell is needed for these feedback-mediated responses, this mechanism of synaptic transmission can modulate the neurotransmitter release in single synaptic terminals without affecting the membrane potential of the entire cell.

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Time dependence of ICl(Ca) in cones with two different [Cl]i. The cones were held at −75 mV and stepped to −50, −40, −30, and −20 mV. For both values of ECl, the current responses are given at 2 min and >20 min after whole-cell configuration was achieved. With ECl at −20 mV, the slowly developing current became inward after an ∼21-min whole-cell configuration (arrow), while it remained outward when ECl was −50 mV.
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Figure 9: Time dependence of ICl(Ca) in cones with two different [Cl]i. The cones were held at −75 mV and stepped to −50, −40, −30, and −20 mV. For both values of ECl, the current responses are given at 2 min and >20 min after whole-cell configuration was achieved. With ECl at −20 mV, the slowly developing current became inward after an ∼21-min whole-cell configuration (arrow), while it remained outward when ECl was −50 mV.

Mentions: Fig. 9 shows the results of two experiments in which the effect of [Cl]i on the sign of ICl(Ca) was studied as a function of time. Since the size of ICl(Ca) varies between the various cones, the cells may not be compared with each other, but changes in ICl(Ca) with time in one individual cell can be used to estimate ECl. Fig. 9 (top) shows the current traces of a cone clamped at various potentials with ECl at −50 mV at 2 and 22 min after achieving whole-cell configuration. In this condition, at both moments in time, a slowly developing outward current can be seen at potentials of −40 mV and above. In both conditions, small tail currents are present. The overall response to the voltage steps does not seem to change dramatically over time. This behavior was observed in all 29 cells tested this way. With ECl at −20 mV, on the other hand, the responses to the same voltage steps strongly change with time (Fig. 9, bottom). At 2 min after achieving whole-cell configuration, only a very small slowly developing outward current can be observed and the tail currents are very small. However, at 21 min, a voltage step to −40 mV induces a large slowly developing inward current and returning back to −75 mV generates a very large tail current. This indicates that ECl has changed strongly during the 20-min whole cell configuration. In all 55 cones tested directly after achieving whole cell configuration, voltage steps to −40 mV never induced a slowly developing inward current and mostly induced a slowly developing outward current. These results indicate that the physiological ECl is about or more negative than −40 mV.


The nature of surround-induced depolarizing responses in goldfish cones.

Kraaij DA, Spekreijse H, Kamermans M - J. Gen. Physiol. (2000)

Time dependence of ICl(Ca) in cones with two different [Cl]i. The cones were held at −75 mV and stepped to −50, −40, −30, and −20 mV. For both values of ECl, the current responses are given at 2 min and >20 min after whole-cell configuration was achieved. With ECl at −20 mV, the slowly developing current became inward after an ∼21-min whole-cell configuration (arrow), while it remained outward when ECl was −50 mV.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1887777&req=5

Figure 9: Time dependence of ICl(Ca) in cones with two different [Cl]i. The cones were held at −75 mV and stepped to −50, −40, −30, and −20 mV. For both values of ECl, the current responses are given at 2 min and >20 min after whole-cell configuration was achieved. With ECl at −20 mV, the slowly developing current became inward after an ∼21-min whole-cell configuration (arrow), while it remained outward when ECl was −50 mV.
Mentions: Fig. 9 shows the results of two experiments in which the effect of [Cl]i on the sign of ICl(Ca) was studied as a function of time. Since the size of ICl(Ca) varies between the various cones, the cells may not be compared with each other, but changes in ICl(Ca) with time in one individual cell can be used to estimate ECl. Fig. 9 (top) shows the current traces of a cone clamped at various potentials with ECl at −50 mV at 2 and 22 min after achieving whole-cell configuration. In this condition, at both moments in time, a slowly developing outward current can be seen at potentials of −40 mV and above. In both conditions, small tail currents are present. The overall response to the voltage steps does not seem to change dramatically over time. This behavior was observed in all 29 cells tested this way. With ECl at −20 mV, on the other hand, the responses to the same voltage steps strongly change with time (Fig. 9, bottom). At 2 min after achieving whole-cell configuration, only a very small slowly developing outward current can be observed and the tail currents are very small. However, at 21 min, a voltage step to −40 mV induces a large slowly developing inward current and returning back to −75 mV generates a very large tail current. This indicates that ECl has changed strongly during the 20-min whole cell configuration. In all 55 cones tested directly after achieving whole cell configuration, voltage steps to −40 mV never induced a slowly developing inward current and mostly induced a slowly developing outward current. These results indicate that the physiological ECl is about or more negative than −40 mV.

Bottom Line: It was found that niflumic acid blocks the feedback-induced depolarizing responses in cones, while the shift of the calcium current activation function and the depolarizing biphasic horizontal cell responses remain intact.Polarization of the presynaptic (horizontal) cell leads to calcium influx in the postsynaptic cell (cone), but due to the combined activity of the calcium current and the calcium-dependent chloride current, the membrane potential of the postsynaptic cell will be hardly modulated, whereas the output of the postsynaptic cell will be strongly modulated.Since no polarization of the postsynaptic cell is needed for these feedback-mediated responses, this mechanism of synaptic transmission can modulate the neurotransmitter release in single synaptic terminals without affecting the membrane potential of the entire cell.

View Article: PubMed Central - PubMed

Affiliation: Graduate School Neurosciences Amsterdam, The Netherlands Ophthalmic Research Institute, 1105 BA Amsterdam, The Netherlands.

ABSTRACT
Cones in the vertebrate retina project to horizontal and bipolar cells and the horizontal cells feedback negatively to cones. This organization forms the basis for the center/surround organization of the bipolar cells, a fundamental step in the visual signal processing. Although the surround responses of bipolar cells have been recorded on many occasions, surprisingly, the underlying surround-induced responses in cones are not easily detected. In this paper, the nature of the surround-induced responses in cones is studied. Horizontal cells feed back to cones by shifting the activation function of the calcium current in cones to more negative potentials. This shift increases the calcium influx, which increases the neurotransmitter release of the cone. In this paper, we will show that under certain conditions, in addition to this increase of neurotransmitter release, a calcium-dependent chloride current will be activated, which polarizes the cone membrane potential. The question is, whether the modulation of the calcium current or the polarization of the cone membrane potential is the major determinant for feedback-mediated responses in second-order neurons. Depolarizing light responses of biphasic horizontal cells are generated by feedback from monophasic horizontal cells to cones. It was found that niflumic acid blocks the feedback-induced depolarizing responses in cones, while the shift of the calcium current activation function and the depolarizing biphasic horizontal cell responses remain intact. This shows that horizontal cells can feed back to cones, without inducing major changes in the cone membrane potential. This makes the feedback synapse from horizontal cells to cones a unique synapse. Polarization of the presynaptic (horizontal) cell leads to calcium influx in the postsynaptic cell (cone), but due to the combined activity of the calcium current and the calcium-dependent chloride current, the membrane potential of the postsynaptic cell will be hardly modulated, whereas the output of the postsynaptic cell will be strongly modulated. Since no polarization of the postsynaptic cell is needed for these feedback-mediated responses, this mechanism of synaptic transmission can modulate the neurotransmitter release in single synaptic terminals without affecting the membrane potential of the entire cell.

Show MeSH
Related in: MedlinePlus