Paradoxical Interaction between Ocular Activity, Perception, and Decision Confidence at the Threshold of Vision

<div><p>In humans and some other species perceptual decision-making is complemented by the ability to make confidence judgements about the certainty of sensory evidence. While both forms of decision process have been studied empirically, the precise relationship between them remains poorly understood. We performed an experiment that combined a perceptual decision-making task (identifying the category of a faint visual stimulus) with a confidence-judgement task (wagering on the accuracy of each perceptual decision). The visual stimulation paradigm required steady fixation, so we used eye-tracking to control for stray eye movements. Our data analyses revealed an unexpected and counterintuitive interaction between the steadiness of fixation (prior to and during stimulation), perceptual decision making, and post-decision wagering: greater variability in gaze direction during fixation was associated with significantly increased visual-perceptual sensitivity, but significantly decreased reliability of confidence judgements. The latter effect could not be explained by a simple change in overall confidence (i.e. a criterion artifact), but rather was tied to a change in the degree to which high wagers predicted correct decisions (i.e. the sensitivity of the confidence judgement). We found no evidence of a differential change in pupil diameter that could account for the effect and thus our results are consistent with fixational eye movements being the relevant covariate. However, we note that small changes in pupil diameter can sometimes cause artefactual fluctuations in measured gaze direction and this possibility could not be fully ruled out. <i>In either case</i>, our results suggest that perceptual decisions and confidence judgements can be processed independently and point toward a new avenue of research into the relationship between them.</p></div

Regions of interest (ROI) analysis of BOLD activity in the nucleus accumbens.

<p>A) Time courses for immediate (dashed) and delayed (solid) choice options in the nucleus accumbens (Nacc, as defined using Talairach atlas). Younger adults (top) are shown in black, older adults (bottom) are shown in grey. B) For younger adults (top) BOLD signal change for immediate choice options in the nucleus accumbens correlates positively with discounting. In contrast, BOLD signal change for delayed choice options correlates negatively with discounting. For older adults (bottom) no significant correlations are obtained.</p

Mean measured gaze direction during trials, averaged across subjects (N = 7).

<p>The sampling rate of our equipment (60 Hz) was not sufficient to resolve individual microsaccades, therefore we used a method that separates trials with extreme variance in gaze direction (OA⁺) from those with relatively stable fixation (OA^-) (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#sec002" target="_blank">Methods</a>). For each subject, we constructed a two-dimensional matrix with each element representing a 0.1° square region on the LCD display. Horizontal and vertical gaze position measurements were binned into the 0.1° x 0.1° square regions, separately for OA⁺ and OA^- trials, and each element of the matrix was assigned the number of times that an eye position was recorded at that location, throughout the entire experiment. Then the grids for all subjects were averaged together to produce panels A and B. (A) Average of trials <i>with</i> high variance in measured gaze direction (OA⁺; identified by looking for outliers in the distribution of velocity measurements across trials. (B) Average of all of the remaining trials (OA^-; i.e. trials <i>without</i> high variance in gaze direction). (C) Difference, <i>with</i> (OA⁺) minus <i>without</i> (OA^-): lighter colors correspond to locations visited more often on OA⁺ trials, and vice versa for darker colors. Note the dark square in the center, indicating that this location was dominated by OA^- trials, and the lighter shades in the periphery indicating that the periphery was dominated by OA⁺ trials. The position data, even <i>with</i> high variance in gaze direction, are confined to a radius of < 1°, consistent with the ocular activity in question being fixational eye movements.</p

Correlation analyses.

<p>A) Correlation between delay discounting (% delayed choices short – long delays) (x-axis) and % BOLD signal change for immediate choice options in the ventral striatum (y-axis). Younger adults are shown in black, older adults are shown in grey. B) Correlation between delay discounting (x-axis) and reaction time for choice options involving delayed reward (y-axis). Younger adults are shown in black, older adults are shown in grey.</p

Behavioral and eye-tracking results.

<p>(A) proportion correct (solid line w/ triangles), proportion of advantageous wagers (<i>PAW</i>, dashed line w/ squares), proportion of high wagers (dotted line w/ circles), and wagering d-prime (<b><i>Wd’</i></b>, dash-dot line w/ x’s). All measures are proportions, except for <b><i>Wd’</i></b>, which is scaled into the range [0,1] for clarity (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#sec002" target="_blank">Methods</a>). Each subject completed 24 trials at each contrast level. (B) Gray line at the top of panel B shows the mean proportion of OA⁺ trials across subjects (scale on the right). Also shown are the mean correlation between OCULAR-ACTIVITY and CORRECT-RESPONSE (solid line with triangles), the mean correlation between OCULAR-ACTIVITY and ADVANTAGEOUS-WAGER (dashed line with squares), and the mean correlation between OCULAR-ACTIVITY and HIGH-WAGER (dotted line with circles). The mean correlation between OCULAR-ACTIVITY and CORRECT-RESPONSE is significantly greater than zero (p = 0.03, two-sided signed-rank test). The mean correlation between OCULAR-ACTIVITY and ADVANTAGEOUS-WAGER is significantly less than zero (p = 0.015, two-sided signed-rank test). The mean correlation between OCULAR-ACTIVITY and HIGH-WAGER was not different from zero (p = 0.44, two-sided signed-rank test). Abbreviations: CD = “correct decision”, AW = “advantageous wager”, HW = “high wager”.</p

Age differences in striatal activity.

<p>A) Left: Significant main effect of age group for choice options involving immediate reward in the ventromedial caudate (t-statistics, significant at p<.05, corrected for multiple comparisons). Right: Time course of BOLD signal change (on the y-axis) for younger (black) and older adults (grey). The x-axis shows time post stimulus onset in seconds. The coordinates refer to Talairach space. B) Left: Significant main effect of age group in the dorsal striatum for all choice options (t-statistics, significant at p<.05, corrected for multiple comparisons). Right: Time course of BOLD signal change (on the y-axis) for younger (black) and older adults (grey). The x-axis shows the repetition time (TR) in seconds. The x-axis shows time post stimulus onset in seconds. The coordinates refer to Talairach space.</p

Time course of the effect at contrast level 2.

<p>In <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#pone.0125278.g003" target="_blank">Fig 3B</a> the correlations between CORRECT RESPONSE and OCULAR ACTIVITY (<b><i>ϕ</i></b>_{<b><i>CR</i></b>}) and between ADVATAGEOUS WAGER and OCULAR ACTIVITY (<b><i>ϕ</i></b>_{<b><i>AW</i></b>}) were computed separately at each contrast level using a fixed 1.5-sec time window starting at stimulus onset (0). In the figure above we mapped the time course of the effect at contrast level 2 using a 1.0-second time window centered on the times shown on the horizontal axis. Stars on the horizontal axis show a series of window positions for which the difference between <b><i>ϕ</i></b>_{<b><i>CR</i></b>} and <b><i>ϕ</i></b>_{<b><i>AW</i></b>} was significant (p < 0.01 corrected, signed rank test, N = 7), and the horizontal bar at the bottom shows the time of visual stimulation (from 0 to 1.333 sec). The effect was largest for windows centered at from 0.5 to 1.0 seconds post-stimulus-onset, consistent with an interaction between small eye movements and stimulus processing. The apparent difference before stimulus onset was not statistically significant.</p

Activity in β-areas and δ- areas across age groups.

<p>Left: Significant activations (t-statistics) for choice pairs involving immediate options (β-areas) averaged across age groups. Talairach coordinates: MFG: -8, 57, 19; vmPFC: 0, 39, -4; PCC: 2, −52, 31. Right: Significant activations for all choice pairs (δ- areas). Activations are significant at p<.05, corrected for multiple comparisons. Talairach coordinates: dlPFC: −42, 36, 22; IFG: −45, 7, 32; Ins: −35, 22, 3; SMA; −1, 15, 48; IPL: 30, −48, 40.</p

Pattern of results for trials with relatively unsteady (OA⁺) and relatively steady (OA^-) gaze direction measurements.

<p>For each subject, the metrics shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#pone.0125278.g003" target="_blank">Fig 3A</a> were computed separately for trials with and trials without detected ocular activity (OA; see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#sec002" target="_blank">Methods</a>). These were then averaged across subjects (N = 7). Labeling of lines is the same as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#pone.0125278.g003" target="_blank">Fig 3A</a>. OA⁺ trials accounted for approximately 70% of trials on average across subjects (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#pone.0125278.g003" target="_blank">Fig 3B</a>).</p

Trial sequence.

<p>Stimuli were presented dichoptically using prism lenses and a cardboard divider (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#pone.0125278.s003" target="_blank">S1 Fig</a>). To the left of the dotted line are the trial sequences from the point of view of each eye, and to the right of the dotted line is the sequence from the subjective point of view showing the resulting fused percept. The visibility of the object depended on the color contrast, which varied from trial to trial. 500ms before stimulus onset, a fixation point appeared (2x2 pixels; < 0.1°) cueing the subject to keep his/her gaze as steady as possible for the next two seconds. In order to limit the possibility of binocular rivalry [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#pone.0125278.ref024" target="_blank">24</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125278#pone.0125278.ref025" target="_blank">25</a>] the stimulus was flashed at a rate of 8 Hz (2 refresh cycles ‘on’ and 6 cycles ‘off’ at 60 Hz refresh rate), for a duration of 1.33 seconds. After stimulus cutoff, the fixation point disappeared and a text prompt appeared cueing the subject to respond (subjects were instructed to wait for the prompt before responding). The first question on each trial was to identify the category of the object by pressing either the ‘F’ (face) or ‘H’ (house) key on a computer keyboard with the left hand, guessing if necessary. Then a second prompt appeared cueing the subject to place a wager (‘high’ = 20¢ or ‘low’ = 5¢) on the accuracy of their immediately preceding perceptual decision, by pressing either the ‘1’ (low bet) or ‘2’ (high bet) key on the numeric key pad with the right hand. If the subject waited longer than 3 seconds to respond, the fixation point would disappear, the inter-trial interval would elapse, and then the next trial would begin. Subjects rarely took longer than 1.5 sec to respond.</p