The structure of large-scale synchronized firing in primate retina

Abstract

Synchronized firing among neurons has been proposed to constitute an elementary aspect of the neural code in sensory and motor systems. However, it remains unclear how synchronized firing affects the large-scale patterns of activity and redundancy of visual signals in a complete population of neurons. We recorded simultaneously from hundreds of retinal ganglion cells in primate retina, and examined synchronized firing in completely sampled populations of approximately 50-100 ON-parasol cells, which form a major projection to the magnocellular layers of the lateral geniculate nucleus. Synchronized firing in pairs of cells was a subset of a much larger pattern of activity that exhibited local, isotropic spatial properties. However, a simple model based solely on interactions between adjacent cells reproduced 99% of the spatial structure and scale of synchronized firing. No more than 20% of the variability in firing of an individual cell was predictable from the activity of its neighbors. These results held both for spontaneous firing and in the presence of independent visual modulation of the firing of each cell. In sum, large-scale synchronized firing in the entire population of ON-parasol cells appears to reflect simple neighbor interactions, rather than a unique visual signal or a highly redundant coding scheme.

Figure 1.

Islands of large-scale synchronized firing in populations of primate ON-parasol RGCs across four preparations (A–D). Each oval represents the 0.9, 1.0, 1.0, and 1.0 SD outline of the Gaussian fit to the receptive field of a single cell in each preparation, respectively. If a neuron spikes within a 10 ms interval, the receptive field is colored black. Shown are six selected frames to highlight the spatial scale of synchronized firing from each preparation under constant illumination (A, B; supplemental Movie 1, available at www.jneurosci.org as supplemental material) and visual stimulation (C, D; supplemental Movie 2, available at www.jneurosci.org as supplemental material).

Figure 2.

Subsampling analysis reveals that 512 electrode recordings capture scale of synchronized firing. Complete mosaic of ON-parasol cells in four preparations (including Fig. 1A,B; see letter labels) is systematically enlarged from center. Black (gray) lines represent mean (±1 SD) across all observed firing patterns. A, Fraction of neurons firing in subsampled population. B, Number of neurons constituting an island of contiguous synchronized firing in subsampled population. C, Fraction of pairs of adjacent cells firing in subsampled population (see Results). Gray bar represents size of multi-neuron firing patterns examined previously (Schneidman et al., 2006; Shlens et al., 2006).

Figure 3.

Large-scale statistical features of neural populations under constant illumination (A) and visual stimulation (B). A, Top row, Distribution of fraction of neurons firing (left), number of contiguous neurons firing (middle), and fraction of adjacent neurons firing (right) in cross-validated data sets (bars) and predicted from statistical independence (dashed line) and pairwise-adjacent model (solid line). Data set is the same as in Figure 1B. Bottom row, Summary comparison between observed probability and prediction from pairwise-adjacent model across four retinas. Each point represents a firing pattern and each color corresponds to one of four retinas. The gray boxes highlight infrequent, large firing patterns encompassing approximately >40% of neurons firing, >15 contiguous neurons firing, or >15% of adjacent cells firing, respectively. B, Same as A, but in the presence of visual stimulation. Top row, The data set from Figure 1D. Bottom row, Summary across 12 retinas. Note logarithmic axes.

Figure 4.

Strength of network interactions. A, Visualization of inferred network architecture in pairwise-adjacent model for Figure 1B. Thickness of red lines indicates the interaction strength (see Materials and Methods). B, Information about firing of four example cells from A available in the surrounding neighborhood as a function of the neighborhood size. C, Comparison of the information about the firing of a single cell contained in small (6 neurons) and large (15 neurons) neighborhoods. Each point represents a single cell and each color corresponds to one of four preparations. D, Comparison of the amount of information about the firing of a single cell in a large neighborhood to the entropy of the individual cell, under constant illumination. Dashed line indicates a slope of 0.2. Colors are the same as in C. E, Same as D, but under white noise visual stimulation. Each color corresponds to 1 of 12 different retinas.