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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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Surround-induced light responses of current-clamped cones to 500-ms flashes of a 3,000-μm surround field (ECl = −20 mV). In control conditions (left), surround stimulation induced depolarizing responses, in 100 μM niflumic acid these responses were absent (middle), and after wash the depolarizing responses recovered slightly (right).
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Figure 6: Surround-induced light responses of current-clamped cones to 500-ms flashes of a 3,000-μm surround field (ECl = −20 mV). In control conditions (left), surround stimulation induced depolarizing responses, in 100 μM niflumic acid these responses were absent (middle), and after wash the depolarizing responses recovered slightly (right).

Mentions: Summarizing: surround stimulation generates a fast inward current (ICa) and, secondary to this, a slowly developing current whose presence depends on the activation of the calcium current. Furthermore, this secondary current can be blocked by niflumic acid and its sign depends on [Cl]i, features that are characteristic for ICl(Ca). Thus the results presented so far suggest that the surround-induced voltage responses of cones are carried by ICl(Ca). If this is indeed the case, then it should be possible to block the surround-induced voltage responses by niflumic acid. Fig. 6 shows the surround-induced voltage responses of a cone with ECl at −30 mV before (left) during (middle), and after (right) application of 100 μM niflumic acid. Niflumic acid had no large effect on the resting membrane potential of the cones, indicating that ICl(Ca) is only slightly activated at physiological membrane potentials. Before application of niflumic acid the cone depolarized ∼15 mV in response to surround stimulation. This response could be blocked completely by niflumic acid and recovered slightly. Similar results were obtained in all nine cells tested this way.


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

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

Surround-induced light responses of current-clamped cones to 500-ms flashes of a 3,000-μm surround field (ECl = −20 mV). In control conditions (left), surround stimulation induced depolarizing responses, in 100 μM niflumic acid these responses were absent (middle), and after wash the depolarizing responses recovered slightly (right).
© Copyright Policy
Related In: Results  -  Collection

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

Figure 6: Surround-induced light responses of current-clamped cones to 500-ms flashes of a 3,000-μm surround field (ECl = −20 mV). In control conditions (left), surround stimulation induced depolarizing responses, in 100 μM niflumic acid these responses were absent (middle), and after wash the depolarizing responses recovered slightly (right).
Mentions: Summarizing: surround stimulation generates a fast inward current (ICa) and, secondary to this, a slowly developing current whose presence depends on the activation of the calcium current. Furthermore, this secondary current can be blocked by niflumic acid and its sign depends on [Cl]i, features that are characteristic for ICl(Ca). Thus the results presented so far suggest that the surround-induced voltage responses of cones are carried by ICl(Ca). If this is indeed the case, then it should be possible to block the surround-induced voltage responses by niflumic acid. Fig. 6 shows the surround-induced voltage responses of a cone with ECl at −30 mV before (left) during (middle), and after (right) application of 100 μM niflumic acid. Niflumic acid had no large effect on the resting membrane potential of the cones, indicating that ICl(Ca) is only slightly activated at physiological membrane potentials. Before application of niflumic acid the cone depolarized ∼15 mV in response to surround stimulation. This response could be blocked completely by niflumic acid and recovered slightly. Similar results were obtained in all nine cells tested this way.

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