Chromatic bipolar cell pathways in the mouse retina

J Neurosci. 2011 Apr 27;31(17):6504-17. doi: 10.1523/JNEUROSCI.0616-11.2011.

Abstract

Like most mammals, mice feature dichromatic color vision based on short (S) and middle (M) wavelength-sensitive cone types. It is thought that mammals share a retinal circuit that in dichromats compares S- and M-cone output to generate blue/green opponent signals, with bipolar cells (BCs) providing separate chromatic channels. Although S-cone-selective ON-BCs (type 9 in mouse) have been anatomically identified, little is known about their counterparts, the M-cone-selective OFF-BCs. Here, we characterized cone connectivity and light responses of selected mouse BC types using immunohistochemistry and electrophysiology. Our anatomical data indicate that four (types 2, 3a/b, and 4) of the five mouse OFF-BCs indiscriminately contact both cone types, whereas type 1 BCs avoid S-cones. Light responses showed that the chromatic tuning of the BCs strongly depended on their position along the dorsoventral axis because of the coexpression gradient of M- and S-opsin found in mice. In dorsal retina, where coexpression is low, most type 2 cells were green biased, with a fraction of cells (≈ 14%) displaying strongly blue-biased responses, likely reflecting S-cone input. Type 1 cells were also green biased but did not comprise blue-biased "outliers," consistent with type 1 BCs avoiding S-cones. We therefore suggest that type 1 represents the green OFF pathway in mouse. In addition, we confirmed that type 9 BCs display blue-ON responses. In ventral retina, all BC types studied here displayed similar blue-biased responses, suggesting that color vision is hampered in ventral retina. In conclusion, our data support an antagonistically organized blue/green circuit as the common basis for mammalian dichromatic color vision.

Publication types

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

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Carrier Proteins / genetics
  • Color
  • Color Perception / physiology
  • Color Vision / physiology*
  • GTPase-Activating Proteins / genetics
  • Green Fluorescent Proteins / genetics
  • Light
  • Mice
  • Mice, Transgenic
  • Microscopy, Confocal
  • Models, Statistical
  • Opsins / metabolism
  • Organophosphorus Compounds / metabolism
  • Peanut Agglutinin / metabolism
  • Phenols / metabolism
  • Photic Stimulation / methods
  • Receptors, Immunologic / genetics
  • Receptors, Neurokinin-3 / genetics
  • Retina / cytology*
  • Retinal Bipolar Cells / classification
  • Retinal Bipolar Cells / physiology*
  • Retinal Cone Photoreceptor Cells / classification
  • Retinal Cone Photoreceptor Cells / physiology*
  • Visual Pathways / physiology*

Substances

  • CLM-1 protein, mouse
  • Carrier Proteins
  • GTPase-Activating Proteins
  • MItoP compound
  • Opsins
  • Organophosphorus Compounds
  • Peanut Agglutinin
  • Phenols
  • Receptors, Immunologic
  • Receptors, Neurokinin-3
  • cytohesin-2
  • Green Fluorescent Proteins