ON and OFF pathways are feature detectors

A key concept in visual system physiology is the notion of “feature detectors.” The idea of feature detection is that the visual system separates the visual image into components, much the way a publisher creates a color print by separating the picture into separate masks for different colored inks. The idea of feature detection was most forcefully presented by Lettvin et al. (1959) in the classic paper, “What the Frog's Eye Tells the Frog's Brain.” In this article, the authors described four different physiological classes of retinal output neurons, that is, four classes of retinal ganglion cells. Ganglion cell axons collectively bundle to form the optic nerve, transmitting visual information to brain visual centers. In this study, each of these classes of ganglion cells was found to be excited by a separate aspect of the visual image. Collectively, the cells sent the visual image to the brain decomposed as four separate channels. Among these four were ON-center and OFF-center cells, ganglion cells selectively specialized for the detection of highlights and shadows.

Clearly, highlights and shadows are two of the most fund-amental features of images. In all vertebrate visual systems studied thus far, highlights and shadows are universally represented, not only by separate sets of ganglion cells, but by separate systems of cells throughout the retina and central nervous system. These are the ON and the OFF pathways. Researchers have come to understand the neural circuitry of these pathways, the cell types that are involved, their morphology and synaptic interconnections, the specialized neurotransmitter systems and receptors used, and the way in which these pathways project to, and are integrated by, the brain.

The lens of the eye projects an optical image of visual space onto the retina. The retina separates this optical image into multiple components. At the outset, this occurs at the photoreceptor level, where rods and cones report different image properties in parallel. Rods deal exclusively with dim signals of slowly varying brightness. Cones deal with bright signals and can detect rapid light fluctuations. Separate cone types sense wavelength with different efficiency, allowing the visual system to detect color. Thus, photoreceptors are the first neurons in the visual chain to decompose the image into separate parts. The image is differentiated further into component elements at the first synapses of the visual pathway: the synapses between photoreceptors and bipolar cells. Here, typically a dozen different bipolar cell types selectively express different types of receptors for glutamate, the neurotransmitter released in light-modulated fashion by photoreceptors. These different glutamate receptors cause each bipolar type to respond to photoreceptor input in a different manner. As with rods and cones, some bipolar cells are tuned to faster fluctuations and some are tuned to slower fluctuations in the visual signal. There are some bipolar cells expressing rapidly desensitizing, rapidly resensitizing AMPA¹ receptors. AMPA¹ is an acronym for ±-α-Amino-hydroxy-5-methylisoxazole-4-propionic acid. There are others expressing the slowly resensitizing kainate receptors. These kinetic differences allow bipolar cells to respond selectively to different temporal components of visual signals (DeVries, 2000). However, the most extraordinary difference occurs between bipolar cells that express excitatory glutamate receptors versus those that express inhibitory glutamate receptors. Inhibitory glutamate receptors are an uncommon class, but are uniquely emphasized in vertebrate retinas. Excitatory and inhibitory glutamate receptors lead to OFF-center and ON-center bipolar cell responses, respectively. Together, these bipolar cells initiate a set of parallel visual pathways, for shadow and for highlight detection. These are the beginnings of the ON- and the OFF-center pathways.