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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 depolarizing responses in a cone with [Cl]i = 50 mM. Occasionally the cone depolarized spontaneously or remained depolarized for a long time (arrow). In this depolarized condition, only small surround-induced responses could be measured (*). The scaling and surround stimulus are indicated in the figure.
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Figure 3: Surround-induced depolarizing responses in a cone with [Cl]i = 50 mM. Occasionally the cone depolarized spontaneously or remained depolarized for a long time (arrow). In this depolarized condition, only small surround-induced responses could be measured (*). The scaling and surround stimulus are indicated in the figure.

Mentions: On some particular occasions, surround-induced responses can become regenerative. Fig. 3 shows the surround-induced responses of a cone with ECl at −20 mV. Sometimes the cone membrane potential did not hyperpolarize after the surround stimulus was turned off (arrow). In this continued depolarized condition, surround stimulation did not induce a significant further depolarization (star). Similar results are obtained in 14 cones as long as ECl is more positive than −30 mV, indicating that in those conditions surround simulation can trigger a regenerative process, which depolarizes the cones to the reversal potential of the current underlying the surround-induced response; i.e., the Cl current. These spontaneous depolarizing responses were never found immediately after achieving whole cell configuration, indicating that under physiological conditions ECl is more negative than −30 mV. It has been suggested that a possible source of this regenerative behavior of the surround-induced responses is the combined activity of ICa and ICl(Ca) (Thoreson and Burkhardt 1991; Barnes and Deschenes 1992). To test this, the currents induced by surround stimulation were studied.


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

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

Surround-induced depolarizing responses in a cone with [Cl]i = 50 mM. Occasionally the cone depolarized spontaneously or remained depolarized for a long time (arrow). In this depolarized condition, only small surround-induced responses could be measured (*). The scaling and surround stimulus are indicated in the figure.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Surround-induced depolarizing responses in a cone with [Cl]i = 50 mM. Occasionally the cone depolarized spontaneously or remained depolarized for a long time (arrow). In this depolarized condition, only small surround-induced responses could be measured (*). The scaling and surround stimulus are indicated in the figure.
Mentions: On some particular occasions, surround-induced responses can become regenerative. Fig. 3 shows the surround-induced responses of a cone with ECl at −20 mV. Sometimes the cone membrane potential did not hyperpolarize after the surround stimulus was turned off (arrow). In this continued depolarized condition, surround stimulation did not induce a significant further depolarization (star). Similar results are obtained in 14 cones as long as ECl is more positive than −30 mV, indicating that in those conditions surround simulation can trigger a regenerative process, which depolarizes the cones to the reversal potential of the current underlying the surround-induced response; i.e., the Cl current. These spontaneous depolarizing responses were never found immediately after achieving whole cell configuration, indicating that under physiological conditions ECl is more negative than −30 mV. It has been suggested that a possible source of this regenerative behavior of the surround-induced responses is the combined activity of ICa and ICl(Ca) (Thoreson and Burkhardt 1991; Barnes and Deschenes 1992). To test this, the currents induced by surround stimulation were studied.

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