Unusual Physiological Properties of Smooth Monostratified Ganglion Cell Types in Primate Retina

Colleen E Rhoades; Nishal P Shah; Michael B Manookin; Nora Brackbill; Alexandra Kling; Georges Goetz; Alexander Sher; Alan M Litke; E J Chichilnisky

doi:10.1016/j.neuron.2019.05.036

Unusual Physiological Properties of Smooth Monostratified Ganglion Cell Types in Primate Retina

Neuron. 2019 Aug 21;103(4):658-672.e6. doi: 10.1016/j.neuron.2019.05.036. Epub 2019 Jun 18.

Authors

Colleen E Rhoades¹, Nishal P Shah², Michael B Manookin³, Nora Brackbill⁴, Alexandra Kling⁵, Georges Goetz⁵, Alexander Sher⁶, Alan M Litke⁶, E J Chichilnisky⁷

Affiliations

¹ Department of Bioengineering, Stanford University, Stanford, CA 94305, USA. Electronic address: crhoades227@gmail.com.
² Department of Electrical Engineering, Stanford University, Stanford, CA 94305, USA.
³ Department of Ophthalmology, University of Washington, Seattle, WA 98195, USA.
⁴ Department of Physics, Stanford University, Stanford, CA 94305, USA.
⁵ Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA; Hansen Experimental Physics Laboratory, Stanford University, Stanford, CA 94305, USA.
⁶ Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.
⁷ Department of Neurosurgery, Stanford University, Stanford, CA 94305, USA; Department of Ophthalmology Stanford University, Stanford, CA 94305, USA; Hansen Experimental Physics Laboratory, Stanford University, Stanford, CA 94305, USA.

Abstract

The functions of the diverse retinal ganglion cell types in primates and the parallel visual pathways they initiate remain poorly understood. Here, unusual physiological and computational properties of the ON and OFF smooth monostratified ganglion cells are explored. Large-scale multi-electrode recordings from 48 macaque retinas revealed that these cells exhibit irregular receptive field structure composed of spatially segregated hotspots, quite different from the classic center-surround model of retinal receptive fields. Surprisingly, visual stimulation of different hotspots in the same cell produced spikes with subtly different spatiotemporal voltage signatures, consistent with a dendritic contribution to hotspot structure. Targeted visual stimulation and computational inference demonstrated strong nonlinear subunit properties associated with each hotspot, supporting a model in which the hotspots apply nonlinearities at a larger spatial scale than bipolar cells. These findings reveal a previously unreported nonlinear mechanism in the output of the primate retina that contributes to signaling spatial information.

Keywords: computation; electrophysiology; retinal ganglion cells; vision.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Action Potentials
Animals
Cell Count
Electrophysiology / methods
Macaca fascicularis
Macaca mulatta
Models, Neurological
Nonlinear Dynamics
Patch-Clamp Techniques
Photic Stimulation
Retinal Ganglion Cells / classification*
Retinal Ganglion Cells / physiology
Retinal Ganglion Cells / radiation effects
Vision, Ocular / physiology

Abstract

Publication types

MeSH terms

Grants and funding