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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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(A) An example of a tail current measurement, 8 min after achieving whole-cell configuration. The cone was recorded with a 33-mM Cl−-containing patch pipette, clamped at −77 mV, stepped to −20 mV for 500 ms, and successively clamped for 400 ms to various potentials. The step to −20 mV activates the ICl(Ca), and the step to the various potentials induces the Ca-dependent tail current. For the estimation of the reversal potential of the tail current, no potentials above −50 mV were used, because at these potentials the activation of the Ca current interferes with the measurements. The difference between the mean current for 50 ms, measured 50 and 300 ms after the step from −20 mV to the various clamp potentials, ranging from −100 up to −50 mV, was used to determine ECl by assuming that the tail current reverses at ECl; i.e., in that condition the difference between the mean current at 50 and 300 ms is zero. (B) Estimation of ECl using the tail-current measurements. The measured ECl's are shown for 11 cells with [Cl] in the pipette (33 mM, •) and for 2 cells with [Cl] in the pipette (7 mM, ○), measured at various moments after achieving the whole-cell configuration. At 2 min, the estimated ECl yields values of approximately ∼55 mV for both values of [Cl]. For the low [Cl], ECl becomes more negative with time, and, for the high [Cl], ECl becomes more positive with time.
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Figure 10: (A) An example of a tail current measurement, 8 min after achieving whole-cell configuration. The cone was recorded with a 33-mM Cl−-containing patch pipette, clamped at −77 mV, stepped to −20 mV for 500 ms, and successively clamped for 400 ms to various potentials. The step to −20 mV activates the ICl(Ca), and the step to the various potentials induces the Ca-dependent tail current. For the estimation of the reversal potential of the tail current, no potentials above −50 mV were used, because at these potentials the activation of the Ca current interferes with the measurements. The difference between the mean current for 50 ms, measured 50 and 300 ms after the step from −20 mV to the various clamp potentials, ranging from −100 up to −50 mV, was used to determine ECl by assuming that the tail current reverses at ECl; i.e., in that condition the difference between the mean current at 50 and 300 ms is zero. (B) Estimation of ECl using the tail-current measurements. The measured ECl's are shown for 11 cells with [Cl] in the pipette (33 mM, •) and for 2 cells with [Cl] in the pipette (7 mM, ○), measured at various moments after achieving the whole-cell configuration. At 2 min, the estimated ECl yields values of approximately ∼55 mV for both values of [Cl]. For the low [Cl], ECl becomes more negative with time, and, for the high [Cl], ECl becomes more positive with time.

Mentions: Since this method to estimate ECl has a limited resolution and works only in the range where ICl(Ca) is activated, a second method for the determination of ECl is needed. Therefore, a second estimate of ECl was made using the tail currents. The experiments of Fig. 8 show that the tail currents can be almost completely blocked by 100 μM niflumic acid, indicating that these currents are carried by ICl(Ca). Fig. 10 shows the current traces of a cone filled with a 33 mM Cl-containing pipette solution 8 min after the whole-cell configuration was achieved. The cone was clamped at −77 mV, stepped to −20 mV for 500 ms and successively clamped for 400 ms to various potentials more negative than −50 mV. The step to −20 mV activates ICa and ICl(Ca), and the subsequent step to negative potentials induces the ICl(Ca)-dependent tail current. For the estimation of the reversal potential of the tail current, no potentials above −50 mV were used because at these potentials the activation of the calcium current interferes with the measurements. To correct for a possible remaining leak current that might be present in the potential range between −100 and −50 mV, the difference between the tail current measured 50 and 300 ms after the step from −20 mV to the negative potentials (gray bars), was used to determine the reversal potential of the tail current. In this way, an estimate of the size of the tail current was obtained for various potentials. In the insert, this estimate is plotted as a function of the potential. The dotted line is a linear curve fitted through the data points using the linear regression algorithm. The intersection with the x axis gives the reversal potential of the tail currents. Since the tail currents are mainly carried by Cl, this value is an estimate of ECl.


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

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

(A) An example of a tail current measurement, 8 min after achieving whole-cell configuration. The cone was recorded with a 33-mM Cl−-containing patch pipette, clamped at −77 mV, stepped to −20 mV for 500 ms, and successively clamped for 400 ms to various potentials. The step to −20 mV activates the ICl(Ca), and the step to the various potentials induces the Ca-dependent tail current. For the estimation of the reversal potential of the tail current, no potentials above −50 mV were used, because at these potentials the activation of the Ca current interferes with the measurements. The difference between the mean current for 50 ms, measured 50 and 300 ms after the step from −20 mV to the various clamp potentials, ranging from −100 up to −50 mV, was used to determine ECl by assuming that the tail current reverses at ECl; i.e., in that condition the difference between the mean current at 50 and 300 ms is zero. (B) Estimation of ECl using the tail-current measurements. The measured ECl's are shown for 11 cells with [Cl] in the pipette (33 mM, •) and for 2 cells with [Cl] in the pipette (7 mM, ○), measured at various moments after achieving the whole-cell configuration. At 2 min, the estimated ECl yields values of approximately ∼55 mV for both values of [Cl]. For the low [Cl], ECl becomes more negative with time, and, for the high [Cl], ECl becomes more positive with time.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC1887777&req=5

Figure 10: (A) An example of a tail current measurement, 8 min after achieving whole-cell configuration. The cone was recorded with a 33-mM Cl−-containing patch pipette, clamped at −77 mV, stepped to −20 mV for 500 ms, and successively clamped for 400 ms to various potentials. The step to −20 mV activates the ICl(Ca), and the step to the various potentials induces the Ca-dependent tail current. For the estimation of the reversal potential of the tail current, no potentials above −50 mV were used, because at these potentials the activation of the Ca current interferes with the measurements. The difference between the mean current for 50 ms, measured 50 and 300 ms after the step from −20 mV to the various clamp potentials, ranging from −100 up to −50 mV, was used to determine ECl by assuming that the tail current reverses at ECl; i.e., in that condition the difference between the mean current at 50 and 300 ms is zero. (B) Estimation of ECl using the tail-current measurements. The measured ECl's are shown for 11 cells with [Cl] in the pipette (33 mM, •) and for 2 cells with [Cl] in the pipette (7 mM, ○), measured at various moments after achieving the whole-cell configuration. At 2 min, the estimated ECl yields values of approximately ∼55 mV for both values of [Cl]. For the low [Cl], ECl becomes more negative with time, and, for the high [Cl], ECl becomes more positive with time.
Mentions: Since this method to estimate ECl has a limited resolution and works only in the range where ICl(Ca) is activated, a second method for the determination of ECl is needed. Therefore, a second estimate of ECl was made using the tail currents. The experiments of Fig. 8 show that the tail currents can be almost completely blocked by 100 μM niflumic acid, indicating that these currents are carried by ICl(Ca). Fig. 10 shows the current traces of a cone filled with a 33 mM Cl-containing pipette solution 8 min after the whole-cell configuration was achieved. The cone was clamped at −77 mV, stepped to −20 mV for 500 ms and successively clamped for 400 ms to various potentials more negative than −50 mV. The step to −20 mV activates ICa and ICl(Ca), and the subsequent step to negative potentials induces the ICl(Ca)-dependent tail current. For the estimation of the reversal potential of the tail current, no potentials above −50 mV were used because at these potentials the activation of the calcium current interferes with the measurements. To correct for a possible remaining leak current that might be present in the potential range between −100 and −50 mV, the difference between the tail current measured 50 and 300 ms after the step from −20 mV to the negative potentials (gray bars), was used to determine the reversal potential of the tail current. In this way, an estimate of the size of the tail current was obtained for various potentials. In the insert, this estimate is plotted as a function of the potential. The dotted line is a linear curve fitted through the data points using the linear regression algorithm. The intersection with the x axis gives the reversal potential of the tail currents. Since the tail currents are mainly carried by Cl, this value is an estimate of ECl.

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