Analysis of the center-surround interaction of rabbit retinal ganglion cells: Physiology and pharmacology

An ubiquitous feature of the receptive fields of sensory neurons is their organization into concentric response areas known as "center" and "surround." Stimulation of the surround leads to two different phenomena. These are the excitatory surround response and the surround's inhibition of the center response. Surround inhibition has been shown to be primarily linear in some cat ganglion cells, but nonlinear in others. This investigation examines the interaction between the center and surround mechanisms of rabbit retinal ganglion cells in an isolated eyecup preparation by stimulating them concurrently, and quantitatively ascertaining the influence of the surround on center responses. The primary tool for this was the construction of response-versus-contrast functions for the center response, with varying luminance contrasts (at various delays), or varying spatial frequency contrast modulations presented to the surround. Additionally, the presence of surround within the center was examined with an identical protocol performed entirely within the center region. Data from these experiments were then modelled with a Michaelis-Menton equation to qualitatively evaluate the inhibitory surround effect for concentric and complex cell types. All protocols show surround inhibition to be primarily nonlinear regardless of ganglion cell type. The surround is most effective when stimulated simultaneously with the center, is spatially low pass and extends into the center region. With the general nature of the center-surround interaction determined, its pharmacological basis was next investigated. This was done in two ways. First, the involvement of the two inhibitory neurotransmitters, gamma-amino butyric acid (GABA) and glycine, was investigated by bath perfusion of their antagonists, picrotoxin and strychnine, during data collection. Surprisingly, neither transmitter seems primarily responsible for surround inhibition. Secondly, the interaction between the ON and OFF channels was examined through the application of 2-amino-4-phosphonobutyric acid (APB), an ON-channel blocker. The contribution of the ON-pathway to the surround of OFF-center cells was determined to be very strong, often accounting for all of the measured surround inhibition.; In summary, then, this investigation utilized response-versus-contrast functions to reveal the nonlinear nature, and cross-channel dependence, of the center-surround interaction in rabbit retinal ganglion cells.