Dynamics of the ganglion cell response in the catfish and frog retinas.

Abstract

Responses were evoked from ganglion cells in catfish and frog retinas by a Gaussian modulation of the mean luminance. An algorithm was devised to decompose intraceUularly recorded responses into the slow and spike components and to extract the time of occurrence of a spike discharge. The dynamics of both signals were analyzed in terms of a series of first-through third-order kernels obtained by cross-correlating the slow (analog) or spike (discrete or point process) signals against the white-noise input. We found that, in the catfish, (a) the slow signals were composed mostly of postsynaptic potentials, (b) their linear components reflected the dynamics found in bipolar cells or in the linear response component of type-N (sustained) amacrine cells, and (c) their nonlinear components were similar to those found in either type-N or type-C (transient) amacrine cells. A comparison of the dynamics of slow and spike signals showed that the characteristic linear and nonlinear dynamics of slow signals were encoded into a spike train, which could be recovered through the cross-correlation between the white-noise input and the spike (point process) signals. In addition, well-defined spike correlates could predict the observed slow potentials. In the spike discharges from frog ganglion cells, the linear (or first-order) kernels were all inhibitory, whereas the second-order kernels had characteristics of on-off transient excitation. The transient and sustained amacrine cells similar to those found in catfish retina were the sources of the nonlinear excitation. We conclude that bipolar cells and possibly the linear part of the type-N cell response are the source of linear, either excitatory or inhibitory, components of the ganglion cell responses, whereas amacrine cells are the source of the cells' static nonlinearity.

Response dynamics and receptive-field organization of catfish ganglion cells [published erratum appears in J Gen Physiol 1995 Aug;106(2):following 388]

“…The third observation shows that there was cross-talk or interference between the center and surround; modulation of the center reduced the sensitivity of the surround. Here we recall that the kernel is a measure of incremental sensitivity (Sakuranaga et al, 1987). We found that the center's response was more robust than the surround's response; the center kernels were less prone to be influenced by the presence of annular modulation.…”

“…Ganglion cells were identified on the basis of their responses to a flash of light and some cells were morphologically identified by injection of dye. We have previously made several functional and morphological studies of catfish ganglion cells (Marmarelis and Naka, 1973;Naka and Can-away, 1975;Davis and Naka, 1980;Sakuranaga, Ando, and Naka, 1987;Naka, 1987a, 1988a, b). The data presented here are cross-referenced to those in our earlier studies.…”

“…Large spike components in intracellular recordings were removed by the process described by Sakuranaga et al (1987). Time resolution of the analysis was 2 ms for both PSPs and spike discharges.…”

“…In visual physiology, in which a nonzero mean luminance is modulated by a white noise, the amplitude as well as waveform of kernels is a function of the luminance and, therefore, is a measure of a cell's incremental (or decremental) sensitivity at the mean luminance (Sakuranaga et al, 1987). From a system in which the output is spike discharges, namely, a point process, a kernel can also be derived by a process of reverse correlation, as originally proposed by de Boer and Kuyper (1968).…”

“…3,4,6,and 7. A more rigorous definition of kernels as a measure of incremental sensitivity can be found elsewhere (Sakuranaga et al, 1987).…”