"Sluggish" Ganglion Cells Fire Precisely and Transmit Information Efficiently

Abstract

Abstract: : Purpose: Sluggish cells constitute half of all ganglion cells in mammalian retina, but their small size (<15 µm soma diameter) makes them harder to record than brisk cells. While brisk cells are known to signal with sparse, precise bursts of spikes ("firing events"), the temporal precision and information content of spike trains from sluggish cells is unknown. Methods: We recorded in "loose patch" mode from brisk and sluggish cells visualized by infrared DIC optics in the intact retina (guinea pig). Cells were characterized as brisk or sluggish based on soma size, peak firing rate to a centered spot, degree of surround inhibition, and autocorrelogram. Each cell was stimulated repeatedly (10-150 trials) with full-field flicker or a spatiotemporally modulated checkerboard (check size and frame rate roughly matched to a cell’s spatiotemporal filter). Temporal precision was measured by the standard deviation of spike time jitter across stimulus trials, and information rates were estimated using the direct method with a time bin of 1 ms and a spike word length of 11 digits. Results: Brisk-transient cells fired to a center spot up to 223 spikes/s (n=2), and brisk-sustained cells fired up to 130 spikes/s (93 ± 34 spikes/s; n=6). During checkerboard or full-field flicker stimulation, the mean firing rate for brisk cells was 19 ± 11 spikes/s and temporal jitter was 10 ± 5 ms. Brisk cells transmitted 2.5 ± 0.9 bits/spike, in agreement with Berry et al., 1997. Sluggish cells fired to a center spot up to 72 spikes/s (48 ± 16 spikes/s; n=5). During checkerboard stimulation, the mean firing rate was 7 ± 3 spikes/s, and the temporal jitter was 10 ± 5 ms. Sluggish cells transmitted 3.9 ± 0.3 bits/spike. Thus sluggish cells transmitted ~50% more bits per spike (Wilcoxon test, p = 0.04). Conclusions: Despite the low peak firing rates and slow response onsets of sluggish cells, their temporal precision is similar to brisk cells. Although sluggish cells transmit fewer bits/s than brisk cells, they transmit with considerably greater efficiency (bits/spike).

Keywords: electrophysiology: non-clinical • ganglion cells • retina: proximal(bipolar, amacrine, and gangli