Kuffler’s study of center-surround retinal ganglion cells

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The classic experiments that Kuffler (1953) performed on retinal ganglion cells have formed the foundations for much of the subsequent physiological analysis of the mammalian visual system. Even beyond the study of vision, they represent a model for understanding the neurobiology of sensory systems. These experiments were performed in vivo in anesthetized cats. The first step in this sort of experiment is the careful placement of a fine microelectrode close to a single neuron so that action potentials can be recorded extracellularly. An oscilloscope trace of the firing pattern of this neuron is important, but the sound of action potentials on an audio monitor is even more critical. This immediate feedback allows the researcher to search for visual stimuli that excite or inhibit the neuron. Kuffler’s first finding was that there were two categories of ganglion cells, as Hartline had seen in the retina of the frog. The cells were either on, i.e., excited by light increment, or off—that is, excited by light decrement.

One of Kuffler’s most important contributions was the careful mapping of lateral interactions in the retina, or what he termed the center-surround structure of the receptive field. When an on ganglion cell was being studied, a small light spot placed in the center of its receptive field would cause an immediate increase in firing rate of the cell (Fig. 26.3B, top). The center of the receptive field of an on ganglion cell was defined as all positions where the small spot evoked an on excitatory response. When the same spot was placed just beyond the center, in the region termed the surround, the neuron decreased its firing rate (Fig. 26.3B, bottom). Kuffler mapped the spatial extent of the regions that evoked excitation or inhibition simply by listening to the responses to spots flashed at many different locations. Alternatively, Kuffler studied receptive fields by searching for an optimal stimulus—one that increased the firing of a ganglion cell most effectively. The strongest stimulus for an on center cell was a spot of light that filled the receptive field center entirely (Fig. 26.3C). Similarly, the most effective inhibitory stimulus was a bright annulus shown to the surround alone. Following such strong inhibition, the cell had an excitatory response when the stimulus was turned off (Fig. 26.3D). Finally, Kuffler studied interactions between receptive field subregions. A large bright stimulus that covered both center and surround was found to evoke a much weaker response than a smaller spot confined to the center; the surround inhibition weakened or altogether eliminated the central excitation (Fig. 26.3E).

Kuffler’s early experiments, along with those of Hartline, established the technical and conceptual foundations for the field of visual physiology. Almost all subsequent work in this field can be seen as falling into the three broad categories of experiments, exemplified by Kuffler’s 1953 study: (1) the mapping of responses with isolated, suboptimal stimuli, (2) the search for an optimal stimulus, and (3) the study of interactions between responses evoked by two or more stimuli.

R. Clay Reid

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