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Vertical interactions across ten parallel, stacked representations in the mammalian retina

Author

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  • Botond Roska

    (University of California at Berkeley, 145 LSA)

  • Frank Werblin

    (University of California at Berkeley, 145 LSA)

Abstract

The mammalian visual system analyses the world through a set of separate spatio-temporal channels1,2. The organization of these channels begins in the retina1,3, where the precise laminations of both the axon terminals of bipolar cells and the dendritic arborizations of ganglion cells suggests the presence of a vertical stack of neural strata at the inner plexiform layer (IPL)3,4,5,6,7,8,9,10,11. Conversely, many inhibitory amacrine cell classes are multiply or diffusely stratified12, indicating that they might convey information between strata. On the basis of the diverse stratification and physiological properties of ganglion cells, it was suggested that the IPL contains a parallel set of representations of the visual world3,7 embodied in the strata and conveyed to higher centres by the classes of ganglion cells whose dendrites ramify at that stratum. Here we show that each stratum receives unique and substantively different excitatory and inhibitory neural inputs that are integrated to form at least ten different, parallel space-time spiking outputs. The response properties of these strata are ordered in the time domain. Inhibition through GABAC receptors extracts spatial edges in neural representations and seems to separate the functional properties of the strata. We describe a new form of neuronal interaction that we call ‘vertical inhibition’ that acts not laterally, but between strata.

Suggested Citation

  • Botond Roska & Frank Werblin, 2001. "Vertical interactions across ten parallel, stacked representations in the mammalian retina," Nature, Nature, vol. 410(6828), pages 583-587, March.
  • Handle: RePEc:nat:nature:v:410:y:2001:i:6828:d:10.1038_35069068
    DOI: 10.1038/35069068
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    Cited by:

    1. Marvin Seifert & Paul A. Roberts & George Kafetzis & Daniel Osorio & Tom Baden, 2023. "Birds multiplex spectral and temporal visual information via retinal On- and Off-channels," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Xiliang Zhang & Sichen Tao & Zheng Tang & Shuxin Zheng & Yoki Todo, 2023. "The Mechanism of Orientation Detection Based on Artificial Visual System for Greyscale Images," Mathematics, MDPI, vol. 11(12), pages 1-13, June.
    3. Sangha Kim & Seongjin Park & Jina Choi & Wonseop Hwang & Sunho Kim & In-Suk Choi & Hyunjung Yi & Rhokyun Kwak, 2022. "An epifluidic electronic patch with spiking sweat clearance for event-driven perspiration monitoring," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Matthew L Katz & Tim J Viney & Konstantin Nikolic, 2016. "Receptive Field Vectors of Genetically-Identified Retinal Ganglion Cells Reveal Cell-Type-Dependent Visual Functions," PLOS ONE, Public Library of Science, vol. 11(2), pages 1-29, February.
    5. Jason S Prentice & Olivier Marre & Mark L Ioffe & Adrianna R Loback & Gašper Tkačik & Michael J Berry II, 2016. "Error-Robust Modes of the Retinal Population Code," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-32, November.
    6. Jen-Chun Hsiang & Ning Shen & Florentina Soto & Daniel Kerschensteiner, 2024. "Distributed feature representations of natural stimuli across parallel retinal pathways," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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