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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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An Amacrine Cell Circuit to Explain Polarity ReversalAn On-Off ganglion cell (G) receives excitatory input (closed circles) from On and Off bipolars (B) in the receptive field center, whose gain is modulated by presynaptic inhibition from amacrine cells (open circles). The peripheral shift depolarizes (see time course above A1) an amacrine cell (A1), which in turn suppresses transmission from the Off bipolar channel. Amacrine A1 also inhibits a second amacrine (A2), which leads to transient disinhibition (see time course above A2) of the On bipolar pathway. See text for details.
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pbio-0050065-g007: An Amacrine Cell Circuit to Explain Polarity ReversalAn On-Off ganglion cell (G) receives excitatory input (closed circles) from On and Off bipolars (B) in the receptive field center, whose gain is modulated by presynaptic inhibition from amacrine cells (open circles). The peripheral shift depolarizes (see time course above A1) an amacrine cell (A1), which in turn suppresses transmission from the Off bipolar channel. Amacrine A1 also inhibits a second amacrine (A2), which leads to transient disinhibition (see time course above A2) of the On bipolar pathway. See text for details.

Mentions: Figure 7 depicts a possible neural circuit that accounts for all the observed effects of a peripheral image shift: polarity reversal in ganglion cells (Figure 2C), slow suppression of the Off pathway (Figures 2, 5, and 6B), and transient enhancement of the On pathway (Figures 2, 5, and 6B). The ganglion cell receives inputs from On and Off bipolar cells. The On bipolar input is tonically suppressed by an amacrine cell (labeled A2), for example, via inhibition at the presynaptic terminal [28,29], and thus the Off inputs dominate. However, an image shift in the periphery stimulates a second amacrine cell (labeled A1), and this neuron in turn suppresses the Off bipolar input through an inhibitory synapse. In addition A1 inhibits A2 [30], which transiently relieves the suppression of the On bipolar inputs. If the synapse from A1 to A2 desensitizes rapidly, then disinhibition of the On pathway would be more transient than suppression of the Off pathway, as observed. When both amacrine cells have regained their resting state, the ganglion cell reverts to its baseline off-dominated response.


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

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

An Amacrine Cell Circuit to Explain Polarity ReversalAn On-Off ganglion cell (G) receives excitatory input (closed circles) from On and Off bipolars (B) in the receptive field center, whose gain is modulated by presynaptic inhibition from amacrine cells (open circles). The peripheral shift depolarizes (see time course above A1) an amacrine cell (A1), which in turn suppresses transmission from the Off bipolar channel. Amacrine A1 also inhibits a second amacrine (A2), which leads to transient disinhibition (see time course above A2) of the On bipolar pathway. See text for details.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0050065-g007: An Amacrine Cell Circuit to Explain Polarity ReversalAn On-Off ganglion cell (G) receives excitatory input (closed circles) from On and Off bipolars (B) in the receptive field center, whose gain is modulated by presynaptic inhibition from amacrine cells (open circles). The peripheral shift depolarizes (see time course above A1) an amacrine cell (A1), which in turn suppresses transmission from the Off bipolar channel. Amacrine A1 also inhibits a second amacrine (A2), which leads to transient disinhibition (see time course above A2) of the On bipolar pathway. See text for details.
Mentions: Figure 7 depicts a possible neural circuit that accounts for all the observed effects of a peripheral image shift: polarity reversal in ganglion cells (Figure 2C), slow suppression of the Off pathway (Figures 2, 5, and 6B), and transient enhancement of the On pathway (Figures 2, 5, and 6B). The ganglion cell receives inputs from On and Off bipolar cells. The On bipolar input is tonically suppressed by an amacrine cell (labeled A2), for example, via inhibition at the presynaptic terminal [28,29], and thus the Off inputs dominate. However, an image shift in the periphery stimulates a second amacrine cell (labeled A1), and this neuron in turn suppresses the Off bipolar input through an inhibitory synapse. In addition A1 inhibits A2 [30], which transiently relieves the suppression of the On bipolar inputs. If the synapse from A1 to A2 desensitizes rapidly, then disinhibition of the On pathway would be more transient than suppression of the Off pathway, as observed. When both amacrine cells have regained their resting state, the ganglion cell reverts to its baseline off-dominated response.

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