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Retinal ganglion cells can rapidly change polarity from Off to On.

Geffen MN, de Vries SE, Meister M - PLoS Biol. (2007)

Bottom Line: The peripheral shift strongly modulates the strength of these two inputs in opposite directions, facilitating the On pathway and suppressing the Off pathway.Furthermore, we identify certain wide-field amacrine cells that contribute to this modulation.This study illustrates how inhibitory interneurons can rapidly gate the flow of information within a circuit, dramatically altering the behavior of the principal neurons in the course of a computation.

View Article: PubMed Central - PubMed

Affiliation: Program in Biophysics, Harvard University, Cambridge, Massachusetts, United States of America.

ABSTRACT
Retinal ganglion cells are commonly classified as On-center or Off-center depending on whether they are excited predominantly by brightening or dimming within the receptive field. Here we report that many ganglion cells in the salamander retina can switch from one response type to the other, depending on stimulus events far from the receptive field. Specifically, a shift of the peripheral image--as produced by a rapid eye movement--causes a brief transition in visual sensitivity from Off-type to On-type for approximately 100 ms. We show that these ganglion cells receive inputs from both On and Off bipolar cells, and the Off inputs are normally dominant. The peripheral shift strongly modulates the strength of these two inputs in opposite directions, facilitating the On pathway and suppressing the Off pathway. Furthermore, we identify certain wide-field amacrine cells that contribute to this modulation. Depolarizing such an amacrine cell affects nearby ganglion cells in the same way as the peripheral image shift, facilitating the On inputs and suppressing the Off inputs. This study illustrates how inhibitory interneurons can rapidly gate the flow of information within a circuit, dramatically altering the behavior of the principal neurons in the course of a computation.

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Some Retinal Ganglion Cells Turn from Off-Center to On-Center following a Peripheral ShiftResponse modulation by the peripheral grating shift is illustrated for three sample ganglion cells: an On cell (A), an Off cell (B), and a polarity-reversing cell (C). Left: changes in firing rate induced by the peripheral shift, displayed as in Figure 1D, bottom. Here and in subsequent figures, the grating shifts of both polarities were averaged. Note that a shift occurred every 0.9 s, so the first and last 0.4 s of these plots are identical. Right: linear filter computed with respect to the flickering spot stimulus in three time periods: the baseline in the 0.4 s preceding the peripheral shift, 0.1–0.2 s after the shift, and 0.3–0.4 s after the shift. The color of the curves corresponds to the time periods on the left.
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pbio-0050065-g002: Some Retinal Ganglion Cells Turn from Off-Center to On-Center following a Peripheral ShiftResponse modulation by the peripheral grating shift is illustrated for three sample ganglion cells: an On cell (A), an Off cell (B), and a polarity-reversing cell (C). Left: changes in firing rate induced by the peripheral shift, displayed as in Figure 1D, bottom. Here and in subsequent figures, the grating shifts of both polarities were averaged. Note that a shift occurred every 0.9 s, so the first and last 0.4 s of these plots are identical. Right: linear filter computed with respect to the flickering spot stimulus in three time periods: the baseline in the 0.4 s preceding the peripheral shift, 0.1–0.2 s after the shift, and 0.3–0.4 s after the shift. The color of the curves corresponds to the time periods on the left.

Mentions: To learn more about the effect of the peripheral shift on local visual processing, we computed the LN model parameters for each ganglion cell in successive 100-ms intervals after the shift [23]. Figure 2A illustrates results that were typical for On-type responses. The filter function shows a biphasic positive peak, indicating that the cell is excited by a dark-to-light transition and fires about 100 ms later. When the peripheral shift occurs, the cell's firing rate is transiently boosted more than 6-fold. However, the filter function remains unchanged during this time, indicating that the neuron always encodes the same stimulus features, though with varying numbers of spikes. A typical Off-type response is illustrated in Figure 2B. This neuron was excited by light-to-dark transitions. The peripheral shift strongly suppressed the firing of this cell, yet the filter function remained unchanged. These cases conform to the classical notion that peripheral image motion modulates the gain of the center response, but not its selectivity.


Retinal ganglion cells can rapidly change polarity from Off to On.

Geffen MN, de Vries SE, Meister M - PLoS Biol. (2007)

Some Retinal Ganglion Cells Turn from Off-Center to On-Center following a Peripheral ShiftResponse modulation by the peripheral grating shift is illustrated for three sample ganglion cells: an On cell (A), an Off cell (B), and a polarity-reversing cell (C). Left: changes in firing rate induced by the peripheral shift, displayed as in Figure 1D, bottom. Here and in subsequent figures, the grating shifts of both polarities were averaged. Note that a shift occurred every 0.9 s, so the first and last 0.4 s of these plots are identical. Right: linear filter computed with respect to the flickering spot stimulus in three time periods: the baseline in the 0.4 s preceding the peripheral shift, 0.1–0.2 s after the shift, and 0.3–0.4 s after the shift. The color of the curves corresponds to the time periods on the left.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1808116&req=5

pbio-0050065-g002: Some Retinal Ganglion Cells Turn from Off-Center to On-Center following a Peripheral ShiftResponse modulation by the peripheral grating shift is illustrated for three sample ganglion cells: an On cell (A), an Off cell (B), and a polarity-reversing cell (C). Left: changes in firing rate induced by the peripheral shift, displayed as in Figure 1D, bottom. Here and in subsequent figures, the grating shifts of both polarities were averaged. Note that a shift occurred every 0.9 s, so the first and last 0.4 s of these plots are identical. Right: linear filter computed with respect to the flickering spot stimulus in three time periods: the baseline in the 0.4 s preceding the peripheral shift, 0.1–0.2 s after the shift, and 0.3–0.4 s after the shift. The color of the curves corresponds to the time periods on the left.
Mentions: To learn more about the effect of the peripheral shift on local visual processing, we computed the LN model parameters for each ganglion cell in successive 100-ms intervals after the shift [23]. Figure 2A illustrates results that were typical for On-type responses. The filter function shows a biphasic positive peak, indicating that the cell is excited by a dark-to-light transition and fires about 100 ms later. When the peripheral shift occurs, the cell's firing rate is transiently boosted more than 6-fold. However, the filter function remains unchanged during this time, indicating that the neuron always encodes the same stimulus features, though with varying numbers of spikes. A typical Off-type response is illustrated in Figure 2B. This neuron was excited by light-to-dark transitions. The peripheral shift strongly suppressed the firing of this cell, yet the filter function remained unchanged. These cases conform to the classical notion that peripheral image motion modulates the gain of the center response, but not its selectivity.

Bottom Line: The peripheral shift strongly modulates the strength of these two inputs in opposite directions, facilitating the On pathway and suppressing the Off pathway.Furthermore, we identify certain wide-field amacrine cells that contribute to this modulation.This study illustrates how inhibitory interneurons can rapidly gate the flow of information within a circuit, dramatically altering the behavior of the principal neurons in the course of a computation.

View Article: PubMed Central - PubMed

Affiliation: Program in Biophysics, Harvard University, Cambridge, Massachusetts, United States of America.

ABSTRACT
Retinal ganglion cells are commonly classified as On-center or Off-center depending on whether they are excited predominantly by brightening or dimming within the receptive field. Here we report that many ganglion cells in the salamander retina can switch from one response type to the other, depending on stimulus events far from the receptive field. Specifically, a shift of the peripheral image--as produced by a rapid eye movement--causes a brief transition in visual sensitivity from Off-type to On-type for approximately 100 ms. We show that these ganglion cells receive inputs from both On and Off bipolar cells, and the Off inputs are normally dominant. The peripheral shift strongly modulates the strength of these two inputs in opposite directions, facilitating the On pathway and suppressing the Off pathway. Furthermore, we identify certain wide-field amacrine cells that contribute to this modulation. Depolarizing such an amacrine cell affects nearby ganglion cells in the same way as the peripheral image shift, facilitating the On inputs and suppressing the Off inputs. This study illustrates how inhibitory interneurons can rapidly gate the flow of information within a circuit, dramatically altering the behavior of the principal neurons in the course of a computation.

Show MeSH
Related in: MedlinePlus