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A simple retinal mechanism contributes to perceptual interactions between rod- and cone-mediated responses in primates.

Grimes WN, Graves LR, Summers MT, Rieke F - Elife (2015)

Bottom Line: Because responses of retinal ganglion cells, the output cells of the retina, depend on signals from both rod and cone photoreceptors, interactions occurring in retinal circuits provide an opportunity to link the mechanistic operation of parallel pathways and perception.Here we show that rod- and cone-mediated responses interact nonlinearly to control the responses of primate retinal ganglion cells; these nonlinear interactions, surprisingly, were asymmetric, with rod responses strongly suppressing subsequent cone responses but not vice-versa.Human psychophysical experiments revealed a similar perceptual asymmetry.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, United States.

ABSTRACT
Visual perception across a broad range of light levels is shaped by interactions between rod- and cone-mediated signals. Because responses of retinal ganglion cells, the output cells of the retina, depend on signals from both rod and cone photoreceptors, interactions occurring in retinal circuits provide an opportunity to link the mechanistic operation of parallel pathways and perception. Here we show that rod- and cone-mediated responses interact nonlinearly to control the responses of primate retinal ganglion cells; these nonlinear interactions, surprisingly, were asymmetric, with rod responses strongly suppressing subsequent cone responses but not vice-versa. Human psychophysical experiments revealed a similar perceptual asymmetry. Nonlinear interactions in the retinal output cells were well-predicted by linear summation of kinetically-distinct rod- and cone-mediated signals followed by a synaptic nonlinearity. These experiments thus reveal how a simple mechanism controlling interactions between parallel pathways shapes circuit output and perception.

No MeSH data available.


Related in: MedlinePlus

Rod → cone interactions in RGC spike output are largely dependent on interactions present in the RGC's excitatory synaptic inputs.(A) Single cell example of rod → cone interactions in spikes (left), excitatory synaptic input (middle) and inhibitory synaptic input (right). (B) Interaction indices (II) for excitatory inputs resembled those observed in spikes. (C) Interactions in inhibitory inputs were highly variable and did not match spike interactions observed in the same cells. (D) Example cell from dynamic-clamp experiments to test contributions of inhibitory synaptic input to rod → cone interactions in spike output. Spike responses elicited by excitatory and inhibitory inputs (left) were compared to those elicited by excitatory inputs alone (right). (E) Population data plotting interaction indices from dynamic-clamp experiments in D. All recordings from whole mount retina.DOI:http://dx.doi.org/10.7554/eLife.08033.004
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fig1s1: Rod → cone interactions in RGC spike output are largely dependent on interactions present in the RGC's excitatory synaptic inputs.(A) Single cell example of rod → cone interactions in spikes (left), excitatory synaptic input (middle) and inhibitory synaptic input (right). (B) Interaction indices (II) for excitatory inputs resembled those observed in spikes. (C) Interactions in inhibitory inputs were highly variable and did not match spike interactions observed in the same cells. (D) Example cell from dynamic-clamp experiments to test contributions of inhibitory synaptic input to rod → cone interactions in spike output. Spike responses elicited by excitatory and inhibitory inputs (left) were compared to those elicited by excitatory inputs alone (right). (E) Population data plotting interaction indices from dynamic-clamp experiments in D. All recordings from whole mount retina.DOI:http://dx.doi.org/10.7554/eLife.08033.004

Mentions: We first compared rod-cone interactions in the output signals of the primate retina with those observed perceptually (Figure 1). We focused on nonlinear interactions between brief increment flashes that preferentially elicited responses from ON retinal circuits; ganglion cell spike outputs in response to these flashes were dominated by excitatory synaptic input (Figure 1—figure supplement 1), further simplifying the circuitry involved. ON parasol ganglion cells (which project to magnocellular layers of the lateral geniculate nucleus) exhibited particularly robust responses to such flashes. We used dim short-wavelength flashes to preferentially activate rod photoreceptors, and brighter long-wavelength flashes to preferentially activate L-cone photoreceptors (Figure 1A,B; Figure 1—figure supplement 2).10.7554/eLife.08033.003Figure 1.Asymmetric nonlinear rod-cone interactions.


A simple retinal mechanism contributes to perceptual interactions between rod- and cone-mediated responses in primates.

Grimes WN, Graves LR, Summers MT, Rieke F - Elife (2015)

Rod → cone interactions in RGC spike output are largely dependent on interactions present in the RGC's excitatory synaptic inputs.(A) Single cell example of rod → cone interactions in spikes (left), excitatory synaptic input (middle) and inhibitory synaptic input (right). (B) Interaction indices (II) for excitatory inputs resembled those observed in spikes. (C) Interactions in inhibitory inputs were highly variable and did not match spike interactions observed in the same cells. (D) Example cell from dynamic-clamp experiments to test contributions of inhibitory synaptic input to rod → cone interactions in spike output. Spike responses elicited by excitatory and inhibitory inputs (left) were compared to those elicited by excitatory inputs alone (right). (E) Population data plotting interaction indices from dynamic-clamp experiments in D. All recordings from whole mount retina.DOI:http://dx.doi.org/10.7554/eLife.08033.004
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4495655&req=5

fig1s1: Rod → cone interactions in RGC spike output are largely dependent on interactions present in the RGC's excitatory synaptic inputs.(A) Single cell example of rod → cone interactions in spikes (left), excitatory synaptic input (middle) and inhibitory synaptic input (right). (B) Interaction indices (II) for excitatory inputs resembled those observed in spikes. (C) Interactions in inhibitory inputs were highly variable and did not match spike interactions observed in the same cells. (D) Example cell from dynamic-clamp experiments to test contributions of inhibitory synaptic input to rod → cone interactions in spike output. Spike responses elicited by excitatory and inhibitory inputs (left) were compared to those elicited by excitatory inputs alone (right). (E) Population data plotting interaction indices from dynamic-clamp experiments in D. All recordings from whole mount retina.DOI:http://dx.doi.org/10.7554/eLife.08033.004
Mentions: We first compared rod-cone interactions in the output signals of the primate retina with those observed perceptually (Figure 1). We focused on nonlinear interactions between brief increment flashes that preferentially elicited responses from ON retinal circuits; ganglion cell spike outputs in response to these flashes were dominated by excitatory synaptic input (Figure 1—figure supplement 1), further simplifying the circuitry involved. ON parasol ganglion cells (which project to magnocellular layers of the lateral geniculate nucleus) exhibited particularly robust responses to such flashes. We used dim short-wavelength flashes to preferentially activate rod photoreceptors, and brighter long-wavelength flashes to preferentially activate L-cone photoreceptors (Figure 1A,B; Figure 1—figure supplement 2).10.7554/eLife.08033.003Figure 1.Asymmetric nonlinear rod-cone interactions.

Bottom Line: Because responses of retinal ganglion cells, the output cells of the retina, depend on signals from both rod and cone photoreceptors, interactions occurring in retinal circuits provide an opportunity to link the mechanistic operation of parallel pathways and perception.Here we show that rod- and cone-mediated responses interact nonlinearly to control the responses of primate retinal ganglion cells; these nonlinear interactions, surprisingly, were asymmetric, with rod responses strongly suppressing subsequent cone responses but not vice-versa.Human psychophysical experiments revealed a similar perceptual asymmetry.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, United States.

ABSTRACT
Visual perception across a broad range of light levels is shaped by interactions between rod- and cone-mediated signals. Because responses of retinal ganglion cells, the output cells of the retina, depend on signals from both rod and cone photoreceptors, interactions occurring in retinal circuits provide an opportunity to link the mechanistic operation of parallel pathways and perception. Here we show that rod- and cone-mediated responses interact nonlinearly to control the responses of primate retinal ganglion cells; these nonlinear interactions, surprisingly, were asymmetric, with rod responses strongly suppressing subsequent cone responses but not vice-versa. Human psychophysical experiments revealed a similar perceptual asymmetry. Nonlinear interactions in the retinal output cells were well-predicted by linear summation of kinetically-distinct rod- and cone-mediated signals followed by a synaptic nonlinearity. These experiments thus reveal how a simple mechanism controlling interactions between parallel pathways shapes circuit output and perception.

No MeSH data available.


Related in: MedlinePlus