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. 2022 Jun 20;32(12):2654-2667.e4.
doi: 10.1016/j.cub.2022.04.067. Epub 2022 May 17.

Perceptual enhancement and suppression correlate with V1 neural activity during active sensing

James E Niemeyer  1 , Seth Akers-Campbell  2 , Aaron Gregoire  3 , Michael A Paradiso  4
Affiliations

Perceptual enhancement and suppression correlate with V1 neural activity during active sensing

James E Niemeyer et al. Curr Biol. .

Abstract

Perception in multiple sensory modalities is an active process that involves exploratory behaviors. In humans and other primates, vision results from sensory sampling guided by saccadic eye movements. Saccades are known to modulate visual perception, and a corollary discharge signal associated with saccades appears to establish a sense of visual stability. Neural recordings have shown that saccades also modulate activity widely across the brain. To investigate the neural basis of saccadic effects on perception, simultaneous recordings from multiple neurons in area V1 were made as animals performed a contrast detection task. Perceptual and neural measures were compared when the animal made real saccades that brought a stimulus into V1 receptive fields and when simulated saccades were made (identical retinal stimulation but no eye movement). When real saccades were made and low spatial frequency stimuli were presented, we observed a reduction in both perceptual sensitivity and neural activity compared with simulated saccades; conversely, with higher spatial frequency stimuli, saccades increased visual sensitivity and neural activity. The performance of neural decoders, which used the activity of the population of simultaneously recorded neurons, showed saccade effects on sensitivity that mirrored the frequency-dependent perceptual changes, suggesting that the V1 population activity could support the perceptual effects. A minority of V1 neurons had significant choice probabilities, and the saccades decreased both average choice probability and pairwise noise correlations. Taken together, the findings suggest that a signal related to saccadic eye movements alters V1 spiking to increase the independence of spiking neurons and bias the system toward processing higher spatial frequencies, presumably to enhance object recognition. The effects of saccades on visual perception and noise correlations appear to parallel effects observed in other sensory modalities, suggesting a general principle of active sensory processing.

Keywords: active perception; choice probability; contrast sensitivity; corollary discharge; efference copy; network covariance; neural decoders; saccadic enhancement; saccadic suppression; sensory-motor integration.

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Conflict of interest statement

Declaration of interests The authors declare no competing interests.

Figures

Figure 1.
Figure 1.. Experimental design.
A) Top view (left) and side view (right) of the experimental apparatus. Two eye trackers were used, one measured the animal’s eye movements (Eye tracker 1) and a second recorded mirror rotations on simulated saccade trials (Eye tracker 2). DM = dichroic mirror, IR = infrared light source. B) 2AFC Task: The color of an initial fixation point indicated trial type. After the initial fixation period in the saccade condition, a saccade target spot appeared, followed by a go cue. In the saccade condition, the animal initiated a saccade to the target and the Gabor stimulus was presented at the site where the V1 receptive fields would land or at a corresponding location in the upper visual field. In the simulated-saccade condition, the animal maintained fixation on the initial fixation target and the mirror rotated; the Gabor stimulus was presented at one of the two same retinotopic locations as in the saccade condition. A 96-channel electrode array recorded V1 neural activity. C) Top: Eye tracker traces from 20 randomly-chosen trials in each animal (0.5 cpd in monkey F and 5 cpd in Monkey M). The pink shaded regions show the time of Gabor onset. Bottom: average traces from the trials above them; shaded area (hardly visible) shows +/− one standard deviation.
Figure 2.
Figure 2.. Perceptual contrast sensitivity.
A) At each spatial frequency, logistic functions were fit to percent correct data in saccade and simulated-saccade conditions. Here, data from animal M at 0.5 and 5 cpd are shown. Contrast threshold was defined as the contrast that gave 70% correct (red dotted lines). B) Contrast sensitivity functions for the saccade (green) and simulated-saccade (black) conditions in both animal subjects. C) Percent change in sensitivity, measured as the percent difference of simulated saccade minus saccade conditions, is shown across frequencies for both animals. Gray shaded region shows where simulated saccade conditions yield better perceptual performance. Green shaded region shows spatial frequencies at which contrast sensitivity was higher in the saccade condition.
Figure 3:
Figure 3:. Neural responses.
A) Single unit examples in monkey M (i) and monkey F (ii) at 0.5 and 5.0 cpd, respectively (Supplemental Figure 1 shows complementary data that reverses the spatial frequencies for the two animals). The cell shown for 0.5 cpd, has a greater response in the simulated saccade condition and the cell shown for 5.0 cpd has a greater response with a real saccade. B) Average population responses for both animals as in (A), N=26 units (i), N=38 units (ii). Shaded regions show +/− one standard error. C) Population data aggregated over all tested contrasts and spatial frequencies. Monkey F on top row, Monkey M bottom row. Scatter plots show simulated saccade condition responses (ordinate) and saccade condition responses (abscissa) for individual cells (Monkey F: N=35, N=32, N=30, N=52, N=40, N=38. Monkey M: N=26, N=28, N=21, N=25, N=21, N=24) across contrast levels. Histograms show deviations from equal responses in the saccade and simulated-saccade conditions (red unity line). Population data statistics: Wilcoxon signed-rank test: * p<0.05; ** p<0.01, *** p<0.001. See also Figure S1.
Figure 4:
Figure 4:. Contrast response functions of single units and population average.
Upper panels: Exemplary single unit responses in saccade (green) and simulated-saccade (black) conditions at 0.5 and 5.0 cpd (lines are Naka-Rushton equation fits). The dotted vertical lines show perceptual contrast thresholds in saccade (green) and simulated-saccade (black) conditions from Figure 2A; N=475 trials (left), N=834 trials (right). Bottom panels: Average population responses (N=35, N=24).
Figure 5:
Figure 5:. Dependence of saccade-based neural response suppression and enhancement on spatial frequency.
A) At each spatial frequency, the average difference between saccade and simulated saccade responses is plotted at the perceptual thresholds established in Figure 2. Purple: thresholds taken from saccade condition; pink, thresholds from simulated saccade condition. Line fit equations are shown for thresholds from simulated saccade condition. Values below zero indicate suppression (gray shading); positive values indicate enhancement in the saccade condition (green shading). B) Percentage of cells with stronger responses in the saccade condition (vs simulated saccade). The responses were taken at the perceptual threshold for contrast obtained in the simulated saccade condition. Line fits are shown with slope estimates for both animals.
Figure 6.
Figure 6.. Animal (dotted lines) and decoder (solid lines) performance at six spatial frequencies and across stimulus contrast.
Decoders were trained on the highest contrast (not shown), which did not serve as a test contrast. Test contrasts vary as they were determined by preliminary behavioral tests to span perceptual threshold at each spatial frequency. With the exception of the lowest contrast, at which behavioral performance approached chance levels, decoder performance generally exceeded behavioral performance. The decoders exhibit the same trends as the animals – performance is worse in the saccade condition at lower spatial frequencies (left panels) and better in the saccade condition at higher spatial frequencies (right panels). Top: animal F, Bottom: animal M.
Figure 7.
Figure 7.. Choice probability and noise correlations in saccade and simulated-saccade conditions.
A) Single-cell choice probabilities for all cells and contrasts in the saccade and simulated-saccade conditions. B) Choice probabilities are significantly higher in the simulated- saccade condition than the saccade condition. C) Pairwise noise correlations in the saccade and simulated saccade conditions and the difference between the two conditions (bottom). The noise correlations are averaged over all neurons and spatial frequencies. See also Table S1.
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Comment in

  • Vision: Optimizing each glimpse.
    Binda P, Morrone MC. Binda P, et al. Curr Biol. 2022 Jun 20;32(12):R567-R569. doi: 10.1016/j.cub.2022.05.025. Curr Biol. 2022. PMID: 35728527

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