NYU/CNSCenter for Neural Science

Contrast dependent biases in pattern motion perception and eye movementRomesh D. Kumbhani1, Miriam Spering 2, J. Anthony Movshon1

1Center for Neural Science, New York University2Dept. of Ophthalmology & Visual Sciences, University of British Columbia

Methodology

Four subjects fixated a centrally located dot for a random time period (500-1000 ms). 50 ms after the fixation point was removed, a large hybrid plaid was presented for 500 ms. The direction and contrast ratio of the hybrid plaid were randomly selected on each trial. Contrast ratios were selected from the following set: 1:1,1:2,1:4,1:8, 1:16, and pure gratings. 100 ms after the stimulus was removed, an arrow was presented pointing in a random initial direction. The subject indicated her perceived direction of motion by rotating the arrow with a trackball; subjects were not given any eye movement instructions. Trials was separated by 1000 ms of mean luminance. Each subject ran 900 trials in 10 equal sessions. The position of each subject’s right eye was recorded with a dual Purkinje-image eye tracker (Fourward Technology), sampled at 1KHz.

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Neurons in area MT signal 2D pattern motion. Their direction selectivity is dependent on the relative contrasts of the elements of a pattern.

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Direction tuning of three MT neurons to hybrid plaids (from Kumbhani et al., 2008, SFN). Blue arrows show the 1D component motion, and red arrows show the 2D pattern motion. As the component contrast ratio increased, direction tuning was dominated by the high-contrast component; at a ratio of 1:4, the tuning was not influenced by the lower-contrast component.

Average eye speed (top) and eye direction (middle) for each hybrid contrast plaid are plotted relative to the onset of the stimulus for subject 1. Error bands are bootstrapped 95% confidence intervals of the mean. The onset of the early OFR was determined by the onset of the eye movement. Prior to this latency, the relative eye direction has no meaning. As the eye entered the early OFR period, we observed a strong bias towards the high-contrast component for contrast ratios > 1. As time progressed, this bias was diminished for ratios less than 1:8. Circular variance (bottom) measures the circular distribution of eye movement directions; a value of 1 indicates random eye motion, while a value of 0 indicates the eye moved in the same direction on each trial. Circular variance begins to fall from 1 at the onset of visually evoked movement. As the eye movement enters the “closed loop” period (~100 ms after early OFR onset), the circular variance plateaus. We designate a late interval in the closed loop period as the tracking interval.

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What are the temporal dynamics of this contrast dependent bias?

Average horizontal and vertical positions and speeds of the eye movements for subject 1 to hybrid-contrast plaids. To show responses to stimuli of the same contrast ratio, all eye directions were rorated with respect to the veridical motion of the stimulus (Adelson & Movshon, 1982), with the veridical motion plotted rightwards. At 1:1 contrast ratio, the eye moved in the veridical direction. For ratios greater than one, direction of eye movement was biased towards the direction of the high-contrast component.

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Do the eyes track the veridical motion of the hybrid plaid?

High-contrast component directionVeridical direction

Adelson EH, Movshon JA(1982). Phenomenal coherence of moving visual patterns. Nature 300:523-525. Distler C, Hoffmann KP (2008). Private lines of cortical visual information to the nucleus of the optic tract and dorsolateral pontine nucleus. Prog Brain Res. 171:363-368.Gellman RS, Carl JR, Miles FA (1990). Short latency ocular-following responses in man. Vis. Neurosci. 5(2):107-122.Kumbhani RD, Saber GT, Majaj NJ, Tailby C, Movshon JA (2008). Contrast affects pattern direction selectivity in macaque MT neurons. SFN Annual meeting, Washington, DC. 460.26/GG18.Miles FA, Kawano K, Optican LM (1986). Short-latency ocular following responses of monkey. I. Dependence on temporospatial properties of visual input. J. Neurophysiol. 56: 1321-1354.Takemura A, Murata Y, Kawano K, Miles FA (2007). Deficits in short-latency tracking eye movements after chemical lesions in monkey cortical areas MT and MST. J Neurosci. 27(3):529-541.

References

We thank Kevin Yen for his assistance in data collection, and members of the Movshon laboratory for their assistance and suggestions regarding data analysis. This work was supported by NIH grants EY02017 and EY04440, and by the Robert Leet and Clara Guthrie Patterson Trust Fellowship.

Acknowledgments

1) The OFRs evoked by hybrid plaids were biased towards the higher-contrast component grating.

2) Across subjects, open loop (early and late OFR) eye movements were more biased by the higher contrast grating than either the closed loop (tracking period) eye movements or the judgments of the perceived motion direction.

3) On a trial-by-trial basis, eye movements during the open loop periods (early and late OFR) did not correlate as well with perception as movements during the closed loop tracking period. Unity gain correlation between eye movements and motion perception increased until ~300 ms, afterwhich it remained constant.

4) The bias of the early OFR matches that found in area MT. Since these biases were stronger than those observed either in the tracking period or perceptual judgments, it is unlikely that the mechanisms involved in generating the OFR directly mediate perception.

Conclusions

Does eye movement direction correlate with perceived direction, trial by trial?

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The trial-by-trial correlation between the eye direction and the perceived direction during the early OFR, late OFR and tracking periods for subject 1. Each dot rep-resents data for a given trial. A tight spread of dots along the line of unity indicates a unity gain correlation between eye movements and perceived direction. To quantify this spread, we subtracted the perceived direction from the eye move-ment direction and fit this distribution to a Gaussian; its standard deviation was used as our measure of spread. On the right, we plot the spread of data around to the line of unity vs. time since stimulus onset; colors represent different con-trast ratios (see left plot). Dashed lines delineate the early OFR, late OFR, and tracking periods. As the eye movements entered the closed looped period, we ob-served a reduction in spread that plateaued ~100 ms after closed loop onset.

For each subject, and each hybrid plaid contrast ratio, we vector averaged the eye movements within the early OFR, late OFR, and tracking periods. Open circles show the mean bias at each contrast ratio for each interval. Error bars are bootstrapped 95% confidence intervals of the mean. In general, the early OFR is strongly biased towards the higher contrast grating, even at a contrast ratio of 2:1. This does not match the bias in perceived motion (where the bias towards the higher contrast grating occurred at contrast ratios greater than 8:1). To quantify the differences in bias, we fit each data set to a cumulative Gaussian and computed the contrast ratio that resulted in a 50% bias in motion direction (CR50). The higher the CR50, the greater the contrast ratio needs to be before significant bias occurs. In the middle, we plot the perceptual CR50 against the oculometric CR50 along with the population means. Relative to perception, the CR50s corresponding to the early OFR period were lower. There was a smooth rightward shift in the CR50s as the interval was closer to the time of the perceived judgment. On the right, we plot the fits to the average biases for each condition for our population. In comparison, the average bias for area MT is shown in white (light gray background traces are biases for individual MT neurons, n=73). The bias during the early OFR period closely matches the bias seen in MT, while the bias during the tracking period matches the perceptual bias.

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Early OFR Late OFR Tracking PerceptionHow variable was the bias across subjects?

What is the ocular following response (OFR)?The ocular following response (OFR) is a reflexive, short latency eye movement evoked by the onset of rapid motion of a large visual stimulus (Miles et al., 1986). Unlike smooth pursuit, which can last as long the stimulus is moving, the OFR persists only for a short duration (~100 ms). On the left are individual (A) and mean (B) eye velocity traces recorded while a subject was viewing a dot field drifting to the right (adapted from Gellmen et al., 1990).

The OFR is mediated by the responses of neurons in area MT via path-ways through the dorsolateral pontine nucleus (DLPN) and the nucleus of the optic tract / accessory optic system (NOT-AOS) (Takemura et al, 2007, Distler and Hoffman, 2008).

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Contactromesh.kumbhani@nyu.eduhttp://www.cns.nyu.edu/~romesh