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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) Light responses of a biphasic horizontal cell, in normal Ringers solution, to 500-ms lasting full-field light stimuli with wavelengths ranging from 500 to 700 nm in 50-nm steps. (B) Biphasic horizontal cell responses to 500-ms lasting full-field light stimuli of 600, 650, and 700 nm. (Left) Depolarizing light responses in control Ringers solution. (Right) Depolarizing light responses recorded in a 100-μM niflumic acid containing Ringers solution.
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Figure 7: (A) Light responses of a biphasic horizontal cell, in normal Ringers solution, to 500-ms lasting full-field light stimuli with wavelengths ranging from 500 to 700 nm in 50-nm steps. (B) Biphasic horizontal cell responses to 500-ms lasting full-field light stimuli of 600, 650, and 700 nm. (Left) Depolarizing light responses in control Ringers solution. (Right) Depolarizing light responses recorded in a 100-μM niflumic acid containing Ringers solution.

Mentions: The results presented so far show that niflumic acid can effectively block the surround-induced depolarizations in cones, without affecting the feedback-induced modulation of ICa. The question now arising is whether the cone depolarization or the modulation of ICa is most important for feedback-induced response in second-order neurons, such as the biphasic horizontal cells (BHCs). The depolarizing responses of the BHCs, due to red light stimulation, are thought to be generated by feedback from the MHCs to the middle wavelength–sensitive cones (Fuortes and Simon 1974; Stell et al. 1975; Stell 1976; Kamermans et al. 1991). Fig. 7 A shows the responses of a BHC to flashes of 500 ms with wavelength ranging from 500 to 700 nm in 50-nm steps. The neutral point, the wavelength where the hyperpolarizing response changes into a depolarizing response, is close to 650 nm. If niflumic acid blocks feedback, then the depolarizing response to 700 nm should be blocked and the neutral point should shift to longer wavelength. Fig. 7 B shows the responses to 650 and 700 nm before and during niflumic acid application. As is clear from this figure, niflumic acid does not block the depolarizing light responses and did not shift the neutral point of the BHC. Although minor changes in the response amplitude were seen occasionally, the feedback-induced responses in BHCs were never blocked in all cells tested (n = 5), whereas the feedback-induced depolarizations in cones were always blocked completely. This experiment shows that depolarization of the cones is not essential for the transmission of a feedback response to second-order neurons.


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

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

(A) Light responses of a biphasic horizontal cell, in normal Ringers solution, to 500-ms lasting full-field light stimuli with wavelengths ranging from 500 to 700 nm in 50-nm steps. (B) Biphasic horizontal cell responses to 500-ms lasting full-field light stimuli of 600, 650, and 700 nm. (Left) Depolarizing light responses in control Ringers solution. (Right) Depolarizing light responses recorded in a 100-μM niflumic acid containing Ringers solution.
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Related In: Results  -  Collection

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Figure 7: (A) Light responses of a biphasic horizontal cell, in normal Ringers solution, to 500-ms lasting full-field light stimuli with wavelengths ranging from 500 to 700 nm in 50-nm steps. (B) Biphasic horizontal cell responses to 500-ms lasting full-field light stimuli of 600, 650, and 700 nm. (Left) Depolarizing light responses in control Ringers solution. (Right) Depolarizing light responses recorded in a 100-μM niflumic acid containing Ringers solution.
Mentions: The results presented so far show that niflumic acid can effectively block the surround-induced depolarizations in cones, without affecting the feedback-induced modulation of ICa. The question now arising is whether the cone depolarization or the modulation of ICa is most important for feedback-induced response in second-order neurons, such as the biphasic horizontal cells (BHCs). The depolarizing responses of the BHCs, due to red light stimulation, are thought to be generated by feedback from the MHCs to the middle wavelength–sensitive cones (Fuortes and Simon 1974; Stell et al. 1975; Stell 1976; Kamermans et al. 1991). Fig. 7 A shows the responses of a BHC to flashes of 500 ms with wavelength ranging from 500 to 700 nm in 50-nm steps. The neutral point, the wavelength where the hyperpolarizing response changes into a depolarizing response, is close to 650 nm. If niflumic acid blocks feedback, then the depolarizing response to 700 nm should be blocked and the neutral point should shift to longer wavelength. Fig. 7 B shows the responses to 650 and 700 nm before and during niflumic acid application. As is clear from this figure, niflumic acid does not block the depolarizing light responses and did not shift the neutral point of the BHC. Although minor changes in the response amplitude were seen occasionally, the feedback-induced responses in BHCs were never blocked in all cells tested (n = 5), whereas the feedback-induced depolarizations in cones were always blocked completely. This experiment shows that depolarization of the cones is not essential for the transmission of a feedback response to second-order neurons.

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