Neuronal and perceptual differences in the temporal processing of darks and lights

Abstract

Visual information is mediated by two major thalamic pathways that signal light decrements (OFF) and increments (ON) in visual scenes, the OFF pathway being faster than the ON. Here, we demonstrate that this OFF temporal advantage is transferred to visual cortex and has a correlate in human perception. OFF-dominated cortical neurons in cats responded ∼3 ms faster to visual stimuli than ON-dominated cortical neurons, and dark-mediated suppression in ON-dominated neurons peaked ∼14 ms faster than light-mediated suppression in OFF-dominated neurons. Consistent with the neuronal differences, human observers were 6-14 ms faster at detecting darks than lights and better at discriminating dark than light flickers. Neuronal and perceptual differences both vanished if backgrounds were biased toward darks. Our results suggest that the cortical OFF pathway is faster than the ON pathway at increasing and suppressing visual responses, and these differences have parallels in the human visual perception of lights and darks.

Figure 1. Recordings from cortical layer 4 in anesthetized cats

Multiple penetrations were made using a 16-channel probe (inter-electrode distance of 100 microns) in V1 of cat visual cortex. The receptive fields were mapped using binary white noise stimuli. (a) The depth of cortical layer 4 was identified as a strong current sink generated by a full-field flash presented at time 0 (left). Cortical receptive fields were measured in layer 4 with binary white noise by spike trigger averaging the stimulus (right). (b) The white noise pixel that generated the strongest response was used to determine the dominance polarity of the cortical receptive field (light for ON-dominated, dark for OFF-dominated). Four time points (latency, peak time, zero-crossing, and suppression time) were chosen to compare the temporal dynamics. (c) The time stamps of the white noise frames with the pixel that generated the strongest response were used as triggers to generate peri-stimulus time-histograms (PSTHs) and rasters for OFF-dominated (blue) and ON-dominated cells (red). The PSTHs were calculated with a 1 ms bin and smoothed using a moving average triangular filter of 21 ms width.

Figure 2. Response time courses of ON-dominated and OFF-dominated multiunit recording sites in cortical layer 4

(a) Mean differences in response time course between ON-dominated (red) and OFF-dominated (blue) layer 4 recordings measured at the four time points described in Figure 1. Error bars show standard errors of mean (** indicates p < 0.001). (b) Distribution of ratios between response suppression and response increment in ON- and OFF-dominated cortical sites. The distributions were fitted with 1D Gaussian functions. Amplitude ratio (AR) was computed as the ratio of suppression amplitude to peak amplitude (S_A / P_A). Integral ratio (IR) (right) was computed as the ratio of the suppression integral to peak integral (S_I / P_I). (c) Fourier transform of the ON and OFF impulse responses represented as normalized power spectra. (d) Peak temporal frequency plotted as a function of signal-to-noise ratio of the dominant (left) and flank subregions (right).

Figure 3. Response time courses of ON-dominated and OFF-dominated single neurons in cortical layer 4

(a) Example of receptive fields from OFF-dominated and ON dominated neurons in cortical layer 4 and spike waveforms (±1 SD envelope). (b) Mean differences in response time course between ON-dominated (red) and OFF-dominated (blue) layer 4 neurons. Error bars show standard errors of mean. * p < 0.05, ** p < 0.01, *** p < 0.005. (c) Distribution of ratios between response suppression and response peak in ON- and OFF-dominated cortical neurons. AR and IR were calculated as in Figure 2. (d) The cortical suppression time is locked to the time when the preferred pixel reverses polarity. (Left) PSTHs from an ON-dominated cortical cell triggered with the time stamps of white-noise stimulus-frames that had the preferred pixel as stimulus onset. In the sequence of white-noise frames, the preferred pixel could last from 2 monitor frames (16.7 ms, black) to 8 monitor frames (66.7 ms, light gray). In this PSTH example, the peak response was very transient and was similar across stimuli, however, the suppression time changed systematically with stimulus duration. The oscillation at the end of the PSTH is a response to the stimulus update (60 Hz), which is characteristic of transient neurons that follow high temporal frequencies. (Right) The stimulus duration was closely related with the relative suppression time with a slope close to 1. The slope was 0.79 for all neurons, 0.75 for ON-dominated (n=15, red circles) and 0.8 for OFF-dominated (n=13, blue circles). This relation is expected if the response suppression is triggered by a reversal in the polarity of the preferred pixel. The relative suppression time was measured as ST_i – ST₁ + 16.7 msec where ST_i is the suppression time for stimulus durationi and ST₁ is the suppression time for a stimulus lasting 16.7 msec.

Figure 4. Cortical responses to dark and light targets on noisy backgrounds

(a) Top panel. The stimuli were large light and dark spots superimposed on a background of binary white noise. The white noise had 2.3 times more light than dark pixels. The dark and light spots were partially superimposed with the population of receptive fields from all cortical sites simultaneously recorded in a single penetration. Gray ellipses are 2D Gaussian fits to cortical receptive fields mapped with sparse noise stimuli. Middle panel. Rasters for 200 trials from a single cortical site in response to dark (blue) and light stimuli (red). Bottom panel. Cortical responses to the stimuli shown at the top, illustrated as PSTHs smoothed with a Gaussian kernel (width = 5 ms). Thin lines show responses of individual recording sites to dark (blue) and light (red) spots and thick lines show the average responses (black for dark spots and gray for light spots). (b) Same as in a, but using white noise with equal number of light and dark pixels. Notice that dark spots generated faster responses than light spots in both a and b. (c) Same as a and b, but using white noise with 0.4 times less light pixels than dark pixels. Notice that the white-noise light/dark ratio had to be reduced for dark and light stimuli to generate responses with similar latency. Interestingly, the value of the light/dark ratio for white noise was similar to the mean dark/light ratio for cortical receptive field size (inset, see methods). The double-peak PSTH is a slow oscillation that we observed when stimulating cortical layer 4 with large stimuli.

Figure 5. Human temporal thresholds in the detection of lights and darks

(a) Observers were presented a pair of targets (one dark, one light) on a uniform noise background (light-to-dark ratio = 0.5), with variable amount of target delay (TD) between them. Size of targets and white noise pixels has been modified for illustration purposes. Observers were asked to report the location of the target that appeared first (light target in this example). (b) Correct responses of three observers to dark (blue) and light (red) targets as a function of TD. Threshold levels were defined as 75% of correct trials (dashed lines). Arrows show the target delay needed to reach the threshold level for dark (blue) and light (red) targets. (c) Thresholds for darks and lights averaged across observers. (d,e,f) Same as (a,b,c) but for uniform noise background adjusted for irradiation illusion (light/dark = 0.4). Error bars show standard errors of mean. Solid lines are psychometric fits to the data points.

Figure 6. Human temporal delay thresholds in the detection of dark and light flickers

(a) Stimulus paradigm. Observers were presented with either dark or light targets on uniform noise background in two consecutive temporal intervals. The figure uses the same ratio of target size to white noise pixel used in experiments. One interval had only one target (single target) and the other had two targets separated by a variable temporal delay (flickering target). Observers were instructed to report the interval in which they perceived a flicker. (b) Proportion of correct responses to dark (blue) and light (red) targets and (c) the average thresholds for three observers. Error bars show standard errors of mean. Solid lines are psychometric fits to the data points.