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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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Population Analysis of Peripheral Shift Effects in On-Off Cells(A) Ratio of spikes caused by the On and Off pathways, before and after the peripheral shift. Each point is for one ganglion cell; open symbols represent cells whose linear filter reversed polarity following the shift. Ratios were computed during the 0.1-s period with the largest effect following the image shift (abscissa) and during the baseline period (ordinate, 0.5–0.9 s after the shift). One polarity-reversing cell is not shown because its responses became purely On-type after the peripheral shift. Colored symbols represent neurons in a retina that was subsequently exposed to APB; in APB, all these cells had an On/Off ratio of zero, regardless of the peripheral shift (not shown). Error bars represent one standard deviation uncertainty in the On/Off ratio (see Materials and Methods).(B) Firing rate produced by the On and Off pathways, as a function of time after the peripheral image shift. The firing rate of each cell was normalized to its time-averaged value, and then averaged over the 149 On-Off cells (top) or over all 248 recorded ganglion cells (bottom). Shaded bands report the standard error of the mean.
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pbio-0050065-g006: Population Analysis of Peripheral Shift Effects in On-Off Cells(A) Ratio of spikes caused by the On and Off pathways, before and after the peripheral shift. Each point is for one ganglion cell; open symbols represent cells whose linear filter reversed polarity following the shift. Ratios were computed during the 0.1-s period with the largest effect following the image shift (abscissa) and during the baseline period (ordinate, 0.5–0.9 s after the shift). One polarity-reversing cell is not shown because its responses became purely On-type after the peripheral shift. Colored symbols represent neurons in a retina that was subsequently exposed to APB; in APB, all these cells had an On/Off ratio of zero, regardless of the peripheral shift (not shown). Error bars represent one standard deviation uncertainty in the On/Off ratio (see Materials and Methods).(B) Firing rate produced by the On and Off pathways, as a function of time after the peripheral image shift. The firing rate of each cell was normalized to its time-averaged value, and then averaged over the 149 On-Off cells (top) or over all 248 recorded ganglion cells (bottom). Shaded bands report the standard error of the mean.

Mentions: The analysis illustrated in Figures 4 and 5 was applied to a sample of 248 ganglion cells, of which 149 cells were driven significantly by both the On and the Off pathway (see Materials and Methods). Among these cells—which we will now call On-Off cells—the relative weighting of the On and Off pathways varied over a wide range of about four orders of magnitude: from 100-fold dominance by Off inputs to 40-fold dominance by On inputs (Figure 6A). Following a peripheral shift, most neurons experienced a transient increase in the On/Off balance. This effect was large: a greater than 2-fold enhancement was seen for 61% of the cells, and a greater than 10-fold change was seen in 19%.


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

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

Population Analysis of Peripheral Shift Effects in On-Off Cells(A) Ratio of spikes caused by the On and Off pathways, before and after the peripheral shift. Each point is for one ganglion cell; open symbols represent cells whose linear filter reversed polarity following the shift. Ratios were computed during the 0.1-s period with the largest effect following the image shift (abscissa) and during the baseline period (ordinate, 0.5–0.9 s after the shift). One polarity-reversing cell is not shown because its responses became purely On-type after the peripheral shift. Colored symbols represent neurons in a retina that was subsequently exposed to APB; in APB, all these cells had an On/Off ratio of zero, regardless of the peripheral shift (not shown). Error bars represent one standard deviation uncertainty in the On/Off ratio (see Materials and Methods).(B) Firing rate produced by the On and Off pathways, as a function of time after the peripheral image shift. The firing rate of each cell was normalized to its time-averaged value, and then averaged over the 149 On-Off cells (top) or over all 248 recorded ganglion cells (bottom). Shaded bands report the standard error of the mean.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0050065-g006: Population Analysis of Peripheral Shift Effects in On-Off Cells(A) Ratio of spikes caused by the On and Off pathways, before and after the peripheral shift. Each point is for one ganglion cell; open symbols represent cells whose linear filter reversed polarity following the shift. Ratios were computed during the 0.1-s period with the largest effect following the image shift (abscissa) and during the baseline period (ordinate, 0.5–0.9 s after the shift). One polarity-reversing cell is not shown because its responses became purely On-type after the peripheral shift. Colored symbols represent neurons in a retina that was subsequently exposed to APB; in APB, all these cells had an On/Off ratio of zero, regardless of the peripheral shift (not shown). Error bars represent one standard deviation uncertainty in the On/Off ratio (see Materials and Methods).(B) Firing rate produced by the On and Off pathways, as a function of time after the peripheral image shift. The firing rate of each cell was normalized to its time-averaged value, and then averaged over the 149 On-Off cells (top) or over all 248 recorded ganglion cells (bottom). Shaded bands report the standard error of the mean.
Mentions: The analysis illustrated in Figures 4 and 5 was applied to a sample of 248 ganglion cells, of which 149 cells were driven significantly by both the On and the Off pathway (see Materials and Methods). Among these cells—which we will now call On-Off cells—the relative weighting of the On and Off pathways varied over a wide range of about four orders of magnitude: from 100-fold dominance by Off inputs to 40-fold dominance by On inputs (Figure 6A). Following a peripheral shift, most neurons experienced a transient increase in the On/Off balance. This effect was large: a greater than 2-fold enhancement was seen for 61% of the cells, and a greater than 10-fold change was seen in 19%.

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