The ON Pathway Rectifies the OFF Pathway of the Mammalian Retina

Abstract

In the vertebrate visual system, ON cells respond to positive contrasts and OFF cells respond to negative contrasts, and thus both ON and OFF cells exhibit rectification. We investigated the retinal circuits by which the ON pathway rectifies the OFF pathway. White noise was projected onto an in vitro preparation of the mammalian retina and excitatory currents were recorded from retinal ganglion cells under whole-cell voltage clamp. Currents in OFF cells were more rectified than those in ON cells: thus, currents in ON cells were able to signal both positive and negative contrasts, but currents in OFF cells were virtually restricted to negative contrasts. Blocking signals in the ON pathway derectified currents in OFF ganglion cells, thus allowing them to be modulated by positive contrasts, indicating that the ON pathway normally rectifies currents in OFF ganglion cells. Such cross-rectification from ON to OFF pathways required intact glycinergic inhibition, indicating that a glycinergic amacrine cell, most likely the AII amacrine cell, allows the ON bipolar cell to hyperpolarize the OFF bipolar cell close to the threshold for transmitter release, thus rectifying excitatory currents in the OFF ganglion cell. Asymmetrical rectification of ON and OFF cells may be an adaptation to natural scenes that have more contrast levels below the mean than above. Thus, in order for ON and OFF pathways to encode an equal number of contrast levels, the ON cells must signal some negative contrasts.