Decision-Related Activity in Macaque V2 for Fine Disparity Discrimination Is Not Compatible with Optimal Linear Readout

Abstract

Fine judgments of stereoscopic depth rely mainly on relative judgments of depth (relative binocular disparity) between objects, rather than judgments of the distance to where the eyes are fixating (absolute disparity). In macaques, visual area V2 is the earliest site in the visual processing hierarchy for which neurons selective for relative disparity have been observed (Thomas et al., 2002). Here, we found that, in macaques trained to perform a fine disparity discrimination task, disparity-selective neurons in V2 were highly selective for the task, and their activity correlated with the animals' perceptual decisions (unexplained by the stimulus). This may partially explain similar correlations reported in downstream areas. Although compatible with a perceptual role of these neurons for the task, the interpretation of such decision-related activity is complicated by the effects of interneuronal "noise" correlations between sensory neurons. Recent work has developed simple predictions to differentiate decoding schemes (Pitkow et al., 2015) without needing measures of noise correlations, and found that data from early sensory areas were compatible with optimal linear readout of populations with informationlimiting correlations. In contrast, our data here deviated significantly from these predictions. We additionally tested this prediction for previously reported results of decision-related activity in V2 for a related task, coarse disparity discrimination (Nienborg and Cumming, 2006), thought to rely on absolute disparity. Although these data followed the predicted pattern, they violated the prediction quantitatively. This suggests that optimal linear decoding of sensory signals is not generally a good predictor of behavior in simple perceptual tasks.

Differentiating between Models of Perceptual Decision Making Using Pupil Size Inferred Confidence

“…Indeed, the difference in mean pupil with available reward size over the last 250 ms of the stimulus presentation was highly statistically reliable ( Fig. 3e), similar to previous findings (Baruni et al, 2015). Previous studies that revealed arousal linked pupil size modulation typically used long intertrial intervals (ITIs) lasting several seconds (Rudebeck et al, 2014;Ebitz and Platt, 2015;Suzuki et al, 2016;Mitz et al, 2017), which were deemed necessary to stabilize pupil size before stimulus or trial onset.…”

“…3a). This analysis yielded qualitatively similar results to bandpass filtering (e.g., Urai et al, 2017) the pupil size data. Finally, pupil size measurements were z-scored using the mean and SD during the stimulus presentation period across all trials.…”

“…Previous work in humans found that pupil size increased with task difficulty, which is thought to reflect changes in arousal related to "cognitive load" or "mental effort" (Hess and Polt, 1964;Kahneman and Beatty, 1966;Alnaes et al, 2014). To explore whether such a signature was evident for our task, we divided our data into easy (Ն50% signal) and hard trials (Ͻ10% signal, excluding 0% signal trials) (Fig.…”

“…5b). Here, we simulated an observer's decision variables on each trial analogously to Urai et al (2017). The decision variable (d) was drawn from a normal distribution whose mean depended on the signed signal strength (with negative and positive signal reflecting near and far stimuli, respectively) and the SD on the observer's internal noise (22.8% signal, the median of the animals' psychophysical thresholds).…”

“…Pupil size has been linked to a subject's arousal in both humans (Bradley et al, 2008) and monkeys (Rudebeck et al, 2014;Ebitz and Platt, 2015;Suzuki et al, 2016;Mitz et al, 2017). Our animals performed a substantial number of trials in each session (mean; Animal A: 828; Animal B: 1067).…”