Directional Summation in Non-direction Selective Retinal Ganglion Cells

Syed Y. Abbas, Khaldoun C. Hamade, Ellen J. Yang, Scott A Nawy, Robert G. Smith, Diana L. Pettit

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Retinal ganglion cells receive inputs from multiple bipolar cells which must be integrated before a decision to fire is made. Theoretical studies have provided clues about how this integration is accomplished but have not directly determined the rules regulating summation of closely timed inputs along single or multiple dendrites. Here we have examined dendritic summation of multiple inputs along On ganglion cell dendrites in whole mount rat retina. We activated inputs at targeted locations by uncaging glutamate sequentially to generate apparent motion along On ganglion cell dendrites in whole mount retina. Summation was directional and dependent13 on input sequence. Input moving away from the soma (centrifugal) resulted in supralinear summation, while activation sequences moving toward the soma (centripetal) were linear. Enhanced summation for centrifugal activation was robust as it was also observed in cultured retinal ganglion cells. This directional summation was dependent on hyperpolarization activated cyclic nucleotide-gated (HCN) channels as blockade with ZD7288 eliminated directionality. A computational model confirms that activation of HCN channels can override a preference for centripetal summation expected from cell anatomy. This type of direction selectivity could play a role in coding movement similar to the axial selectivity seen in locust ganglion cells which detect looming stimuli. More generally, these results suggest that non-directional retinal ganglion cells can discriminate between input sequences independent of the retina network.

Original languageEnglish (US)
Article numbere1002969
JournalPLoS Computational Biology
Volume9
Issue number3
DOIs
StatePublished - Apr 15 2013

Fingerprint

Retinal Ganglion Cells
Summation
Chemical activation
Dendrites
Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
locust
Ganglia
Cell
Retina
theoretical study
anatomy
Dendrite
Carisoprodol
dendrites
retina
cells
Activation
cyclic nucleotides
Rats
Fires

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Modeling and Simulation
  • Ecology
  • Molecular Biology
  • Genetics
  • Cellular and Molecular Neuroscience
  • Computational Theory and Mathematics

Cite this

Abbas, S. Y., Hamade, K. C., Yang, E. J., Nawy, S. A., Smith, R. G., & Pettit, D. L. (2013). Directional Summation in Non-direction Selective Retinal Ganglion Cells. PLoS Computational Biology, 9(3), [e1002969]. https://doi.org/10.1371/journal.pcbi.1002969

Directional Summation in Non-direction Selective Retinal Ganglion Cells. / Abbas, Syed Y.; Hamade, Khaldoun C.; Yang, Ellen J.; Nawy, Scott A; Smith, Robert G.; Pettit, Diana L.

In: PLoS Computational Biology, Vol. 9, No. 3, e1002969, 15.04.2013.

Research output: Contribution to journalArticle

Abbas, SY, Hamade, KC, Yang, EJ, Nawy, SA, Smith, RG & Pettit, DL 2013, 'Directional Summation in Non-direction Selective Retinal Ganglion Cells', PLoS Computational Biology, vol. 9, no. 3, e1002969. https://doi.org/10.1371/journal.pcbi.1002969
Abbas, Syed Y. ; Hamade, Khaldoun C. ; Yang, Ellen J. ; Nawy, Scott A ; Smith, Robert G. ; Pettit, Diana L. / Directional Summation in Non-direction Selective Retinal Ganglion Cells. In: PLoS Computational Biology. 2013 ; Vol. 9, No. 3.
@article{9296446f663d43499fd45ed1440978bd,
title = "Directional Summation in Non-direction Selective Retinal Ganglion Cells",
abstract = "Retinal ganglion cells receive inputs from multiple bipolar cells which must be integrated before a decision to fire is made. Theoretical studies have provided clues about how this integration is accomplished but have not directly determined the rules regulating summation of closely timed inputs along single or multiple dendrites. Here we have examined dendritic summation of multiple inputs along On ganglion cell dendrites in whole mount rat retina. We activated inputs at targeted locations by uncaging glutamate sequentially to generate apparent motion along On ganglion cell dendrites in whole mount retina. Summation was directional and dependent13 on input sequence. Input moving away from the soma (centrifugal) resulted in supralinear summation, while activation sequences moving toward the soma (centripetal) were linear. Enhanced summation for centrifugal activation was robust as it was also observed in cultured retinal ganglion cells. This directional summation was dependent on hyperpolarization activated cyclic nucleotide-gated (HCN) channels as blockade with ZD7288 eliminated directionality. A computational model confirms that activation of HCN channels can override a preference for centripetal summation expected from cell anatomy. This type of direction selectivity could play a role in coding movement similar to the axial selectivity seen in locust ganglion cells which detect looming stimuli. More generally, these results suggest that non-directional retinal ganglion cells can discriminate between input sequences independent of the retina network.",
author = "Abbas, {Syed Y.} and Hamade, {Khaldoun C.} and Yang, {Ellen J.} and Nawy, {Scott A} and Smith, {Robert G.} and Pettit, {Diana L.}",
year = "2013",
month = "4",
day = "15",
doi = "10.1371/journal.pcbi.1002969",
language = "English (US)",
volume = "9",
journal = "PLoS Computational Biology",
issn = "1553-734X",
publisher = "Public Library of Science",
number = "3",

}

TY - JOUR

T1 - Directional Summation in Non-direction Selective Retinal Ganglion Cells

AU - Abbas, Syed Y.

AU - Hamade, Khaldoun C.

AU - Yang, Ellen J.

AU - Nawy, Scott A

AU - Smith, Robert G.

AU - Pettit, Diana L.

PY - 2013/4/15

Y1 - 2013/4/15

N2 - Retinal ganglion cells receive inputs from multiple bipolar cells which must be integrated before a decision to fire is made. Theoretical studies have provided clues about how this integration is accomplished but have not directly determined the rules regulating summation of closely timed inputs along single or multiple dendrites. Here we have examined dendritic summation of multiple inputs along On ganglion cell dendrites in whole mount rat retina. We activated inputs at targeted locations by uncaging glutamate sequentially to generate apparent motion along On ganglion cell dendrites in whole mount retina. Summation was directional and dependent13 on input sequence. Input moving away from the soma (centrifugal) resulted in supralinear summation, while activation sequences moving toward the soma (centripetal) were linear. Enhanced summation for centrifugal activation was robust as it was also observed in cultured retinal ganglion cells. This directional summation was dependent on hyperpolarization activated cyclic nucleotide-gated (HCN) channels as blockade with ZD7288 eliminated directionality. A computational model confirms that activation of HCN channels can override a preference for centripetal summation expected from cell anatomy. This type of direction selectivity could play a role in coding movement similar to the axial selectivity seen in locust ganglion cells which detect looming stimuli. More generally, these results suggest that non-directional retinal ganglion cells can discriminate between input sequences independent of the retina network.

AB - Retinal ganglion cells receive inputs from multiple bipolar cells which must be integrated before a decision to fire is made. Theoretical studies have provided clues about how this integration is accomplished but have not directly determined the rules regulating summation of closely timed inputs along single or multiple dendrites. Here we have examined dendritic summation of multiple inputs along On ganglion cell dendrites in whole mount rat retina. We activated inputs at targeted locations by uncaging glutamate sequentially to generate apparent motion along On ganglion cell dendrites in whole mount retina. Summation was directional and dependent13 on input sequence. Input moving away from the soma (centrifugal) resulted in supralinear summation, while activation sequences moving toward the soma (centripetal) were linear. Enhanced summation for centrifugal activation was robust as it was also observed in cultured retinal ganglion cells. This directional summation was dependent on hyperpolarization activated cyclic nucleotide-gated (HCN) channels as blockade with ZD7288 eliminated directionality. A computational model confirms that activation of HCN channels can override a preference for centripetal summation expected from cell anatomy. This type of direction selectivity could play a role in coding movement similar to the axial selectivity seen in locust ganglion cells which detect looming stimuli. More generally, these results suggest that non-directional retinal ganglion cells can discriminate between input sequences independent of the retina network.

UR - http://www.scopus.com/inward/record.url?scp=84875976950&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84875976950&partnerID=8YFLogxK

U2 - 10.1371/journal.pcbi.1002969

DO - 10.1371/journal.pcbi.1002969

M3 - Article

VL - 9

JO - PLoS Computational Biology

JF - PLoS Computational Biology

SN - 1553-734X

IS - 3

M1 - e1002969

ER -