Faster thalamocortical processing for dark than light visual targets

Abstract

ON and OFF visual pathways originate in the retina at the synapse between photoreceptor and bipolar cells. OFF bipolar cells are shorter in length and use receptors with faster kinetics than ON bipolar cells and, therefore, process information faster. Here, we demonstrate that this temporal advantage is maintained through thalamocortical processing, with OFF visual responses reaching cortex ~3-6 ms before ON visual responses. Faster OFF visual responses could be demonstrated in recordings from large populations of cat thalamic neurons representing the center of vision (both X and Y) and from subpopulations making connection with the same cortical orientation column. While the OFF temporal advantage diminished as visual responses reached their peak, the integral of the impulse response was greater in OFF than ON neurons. Given the stimulus preferences from OFF and ON channels, our results indicate that darks are processed faster than lights in the thalamocortical pathway.

Figure 1.

Example of two simultaneously recorded Y geniculate neurons, illustrating a faster response time course in OFF than ON. a, Spatiotemporal receptive field movies of the two Y cells (solid red lines, ON; dotted blue lines, OFF). Each frame represents the receptive field at a specific time delay between stimulus and response (frame 0 shows the response between 0 and 16 ms, frame 16 shows the response between 16 and 33 ms, and so on). In this example, as in most geniculate cells, the response peak was followed by a strong rebound due to the change in the contrast polarity of the stimulus (solid blue lines, ON rebound in OFF cell; dotted red lines, OFF rebound in ON cell). b, Biphasic response time course of the two LGN neurons (blue, OFF; red, ON). Response time was measured at four different points: at 40% of the peak from the first rising phase (response latency), at the peak of the first phase (peak time), at the zero crossing between phases (zero-crossing), and at the peak of the second phase (rebound time).

Figure 2.

Receptive fields and response latencies of an LGN cell population, illustrating faster OFF than ON visual responses. a, Most cells responding 16–33 ms after stimulus onset were OFF cells. The receptive field of each cell is illustrated by a contour line containing the region that generated responses >20% of the maximum. b, ON and OFF cells responded in equal number at 33–49 ms. c, d, Receptive field center positions (position of visual space that generated the maximum response in each cell). AC, Area centralis.

Figure 3.

The average response latency is ∼4 ms shorter in OFF than ON geniculate cells. a, Examples of rasters and impulse responses from OFF (top) and ON (bottom) cells. The rasters are aligned with the onset of the preferred white noise pixel for each cell (the pixel with the polarity and position that generated the maximum response). Bin width for impulse responses was 1 ms. b, On average, OFF geniculate cells had shorter response latencies and peak times than ON geniculate cells (average latency difference: 3.84 ms; average peak-time difference: 2.6 ms, p < 0.001, Mann–Whitney test). Differences in zero-crossing and rebound time were not significant. Sample size: 548 LGN cells were recorded in nine different animals (OFF: n = 258, ON: n = 290). c, Distributions of response latency and peak time fitted with Gaussian functions.

Figure 4.

The response latency was ∼6 ms shorter in Y-OFF than Y-ON cells and ∼3 ms shorter in X-OFF than X-ON cells. a, Examples of rasters and impulse responses from all four different cell types. b, OFF geniculate cells had shorter response latencies than ON geniculate cells in both the X and Y pathways (average latency difference X-ON–X-OFF: 3.0 ms; Y-ON–Y-OFF: 5.93 ms, p < 0.001, Mann–Whitney test). This analysis included 302 X and 158 Y LGN cells (233 OFF, 227 ON).

Figure 5.

Response latency differences between OFF and ON geniculate cells making monosynaptic connection within the same cortical orientation column. a, Examples from two geniculate cells making monosynaptic connection with two different orientation columns in visual cortex. The left one made monosynaptic connection in cortical layer 4 and the right one in both layers 4 and 6. STLFP, Spike-triggered local field potential; STCSD, spike-triggered current-source-density. b–d, Measurements of response time course in three different orientation columns. In two cortical orientation columns, OFF had significantly faster response latency than ON by 1.53 ms (b) and 2.4 ms (c). In the third column (d), OFF was also faster but the difference was not significant. In two of the columns, we also found significant differences in rebound time (b) and peak time (c). e, In the total sample, the response latency was 1.7 ms shorter to the onset of dark stimuli in OFF than the onset of light stimuli in ON cells. ON cells also reduced their responses 4.1 ms faster when a light pixel turned dark than OFF cells did when a dark pixel turned light.

Figure 6.

The rebound of the impulse response is stronger in ON than OFF geniculate neurons. Top, The biphasic index (BI), calculated as a rebound/peak amplitude ratio, was 12% significantly larger in ON than OFF neurons (0.536 vs 0.479, p = 0.00001, Mann–Whitney test). Bottom, The rebound index (RI), calculated as a rebound/peak area ratio was 30% significantly larger in ON than OFF neurons (1.133 vs 0.869, p = 0.00001, Mann–Whitney test).