Location- and feature-based selection histories make independent, qualitatively distinct contributions to urgent visuomotor performance

Abstract

Attention mechanisms guide visuomotor behavior by weighing physical salience and internal goals to prioritize stimuli as choices for action. Although less well studied, selection history, which reflects multiple facets of experience with recent events, is increasingly recognized as a distinct source of attentional bias. To examine how selection history impacts saccadic choices, we trained two macaque monkeys to perform an urgent version of an oddball search task in which a red target appeared among three green distracters, or vice versa. By imposing urgency, performance could be tracked continuously as it transitioned from uninformed guesses to informed choices as a function of processing time. This, in turn, permitted assessment of attentional control as manifest in motor biases, processing speed, and asymptotic accuracy. Here, we found that the probability of making a correct choice was strongly modulated by the histories of preceding target locations and target colors. Crucially, although both effects were gated by success (or reward), their dynamics were clearly distinct: whereas location history promoted a motor bias, color history modulated perceptual sensitivity, and these influences acted independently. Thus, combined selection histories can give rise to enormous swings in visuomotor performance even in simple tasks with highly discriminable stimuli.

Figure 1.

Behavioral task and psychophysical performance from two monkeys. (a) The compelled oddball (CO) task. Trials begin when the subject fixates on the central gray spot (Fixation). Four gray placeholders then appear (Targets On) separated by 90° surrounding the fixation spot (at variable eccentricities and orientations across days). Urgency is incorporated by next extinguishing the fixation spot (Go), which instructs the subject to respond. After a variable time delay (Gap, 0–225 ms), the target and distracter identities are revealed (Cue). A correct choice requires a saccade to the stimulus with a unique color, the oddball stimulus, within 450 ms of the go signal. The reaction time (RT) is measured from the go signal to saccade onset. The processing time (PT) interval is the maximum amount of time during which the cue can inform the choice. (b) Tachometric curves showing the percentage of correct responses as a function of PT for monkey C (top; 26,038 trials) and monkey N (bottom; 45,173 trials). Gray shades represent 95% confidence intervals (CIs). Chance performance (25%) is indicated by dotted lines. PT bin size is 50 ms. (c) Mean percentage of correct choices as a function of gap for monkey C (top) and monkey N (bottom). Error bars indicate 95% CIs. (d) Mean RT as a function of gap for monkey C (top) and monkey N (bottom). Error bars indicate ± 1 standard deviation.

Figure 2.

Repetitions and switches of target color and target location cause distinct modulations of performance in the CO task. Each panel shows results for performance on the current trial conditioned on the history of preceding trials when current and past trials are the same (S, blue spectrum; color or location repeats) or different (D, red spectrum; color or location switches). Both S and D sequences go back 1–4 trials into the past. (a) Tachometric curves conditioned on target color history. Performance is shown as a function of PT for eight different history sequences. Average performance is shown in gray. Bin width is 50 ms for all curves. For clarity, error bars are omitted. (b) Choice accuracy (x axis, percent correct) in short-PT trials (PT < 100 ms, floor) conditioned on color history (y axis). Error bars represent 95% CIs across trials. Gray vertical line denotes value for the average tachometric curve. (c) Choice accuracy in long-PT trials (PT > 150 ms, ceiling) conditioned on color history. Same format as in b. (d) Average RT (x axis, in ms) conditioned on color history (y axis). Error bars show ± 1 standard error of the mean (SEM). The gray vertical line denotes average RT across all trials. (e) Tachometric curves conditioned on target location history. (f) Choice accuracy in short-PT trials (PT < 100 ms, floor) conditioned on location history. (g) Choice accuracy in long-PT trials (PT > 150 ms, ceiling) conditioned on location history. (h) Average RT conditioned on location history.

Figure 3.

History effects due to target color and target location have distinct temporal manifestations within the timecourse of a trial. Each curve plots the difference between two tachometric curves, one conditioned on same (S) trials and another conditioned on different (D) trials. Each panel shows two difference curves, one for color history (gold traces) and another for location history (black traces), with shaded error bands indicating ± 1 SE across trials. Dotted lines at zero mark no difference in performance given S and D histories. (a) Difference curves for histories going back 1 trial (1S – 1D). (b) Difference curves for histories going back 2 trials (2S – 2D). (c) Difference curves for histories going back 3 trials (3S – 3D). (d) Difference curves for histories going back 4 trials (4S – 4D). Note that the location bias is strongest at short PTs and then declines, whereas the color bias rises sharply after ~100 ms of PT.

Figure 4.

The timescale of history effects induced by a single repeat or a single switch varies across history types. (a) Task performance during uninformed choices (floor, percent correct) following a single color repetition (1S; blue axis) or color switch (1D; brown axis) that occurred 1–10 trials prior to the trial being evaluated. The notation Nx indicates N intervening trials of any type between the first event and the repeat or switch. (b) As in a, but for performance during informed choices (ceiling). (c) Task performance during uninformed choices (floor, percent correct) following a target location repetition (1S, blue axis) or target location switch (1D, red axis) that occurred 1–10 trials prior to the trial being evaluated. (d) As in c, but for performance during informed choices (ceiling). In all plots, error bars represent 95% CIs.

Figure 5.

Perceptual accuracy is strongly modulated by the joint history of target color and trial outcome. (a–d) Task performance in color repeats. Data are conditioned on the histories of preceding trials having the same target color (S) and resulting in either correct (C, green spectrum; 1–4 preceding correct trials) or error outcomes (E, purple spectrum; 1–4 preceding error trials). (e–h) Task performance in color switches. Data are conditioned on the histories of preceding trials having a different (D) target color and resulting in either correct (C, green spectrum; 1–4 preceding correct trials) or error outcomes (E, purple spectrum; 1–4 preceding error trials). Formatting for the tachometric curves (a, e), floor accuracies (b, f), ceiling accuracies (c, g), and mean RTs (d, h) is the same as in Fig. 2. The gray shaded areas in a and e indicate ranges of history effects obtained without taking outcome history into account, for color repeats (from 1S–4S in Fig. 2a, blue curves) and color switches (from 1D–4D in Fig. 2a, red curves), respectively.

Figure 6.

Motor bias is strongly modulated by the joint history of target location and trial outcome. The format of this figure is exactly the same as that of Fig. 5, except that it considers the joint history of target location and trial outcome (rather than target color and trial outcome). The gray shaded areas in a and e indicate ranges of history effects obtained without taking outcome history into account, for location repeats (from 1S–4S in Fig. 2e, blue curves) and location switches (from 1D–4D in Fig. 2e, red curves), respectively.

Figure 7.

Tests of interaction between individual histories. Each panel plots the predicted task performance at long PTs (ceiling accuracy) based upon independent contributions from two history effects (y axis), contrasted with the actual, measured task performance (x axis). Rows correspond to comparisons based on histories going 1, 2, 3, or 4 trials back (H, from top to bottom). Each point represents one specific history sequence. Labels in top panels identify a few combined history sequences in each case. Error bars represent 95% CIs. Red and black identify individual points with CI spans smaller (red) or larger (black) than 15 percentage points, which divides the data into high- and low-reliability points. Regression lines based on the red points are plotted in blue, with the slope (β₂) and its 95% CI indicated in each case. Dotted diagonal lines indicate equality. Note that the overall probability of success across all trials is 66% correct. (a) Interaction between target color and target location histories. (b) Interaction between target color and outcome histories. (c) Interaction between target location and outcome histories. (d) Interaction between target color and target location histories, each combined with outcome. Note that the joint effect of color and location histories is highly predictable based on their individual effects on performance.

Figure 8.

Consistency of history effects across individual subjects. The data in this figure are analogous to the bar plots shown in Figs. 2, 5, and 6, but for each of the two monkeys. In each panel, the x axis indicates specific history sequences (see labels in c). On the y axes, orange filled circles are results from monkey C and open circles are from monkey N. For clarity, the two sets of data points are slightly offset from each other along the x axis. Blue error bars indicate 95% CIs across trials. (a) Choice accuracy (percent correct) in short-PT trials (PT < 100 ms, floor) conditioned on each history sequence. The dotted line marks chance performance (25% correct). (b) Choice accuracy (percent correct) in long-PT trials (PT > 150 ms, ceiling) conditioned on each history sequence. The dotted line marks average performance for informed choices (66% correct). (c) Mean RT conditioned on each history sequence. Data points include all trials in each condition (correct and incorrect, all PTs). The dotted lines mark the overall mean RTs for the two monkeys (with the RTs of monkey N shifted by −29 ms; Methods).

Figure 1 — figure supplement 1.

Variability in performance across animals and rule sets. (a, b) Task performance for monkey C (a) and monkey N (b) in the current study; during the CO task, target colors and locations were randomly sampled across trials. Tachometric curves show performance on the current trial conditioned on the histories of preceding trials having the same target color (S, blue spectrum; 1S–4S sequences; dark to light) or a different target color (D, red spectrum; 1D–4D sequences; dark to light). (c) Task performance for monkey I from a previous study (Scerra et al., 2019). This subject ran a version of the CO task in which target locations were randomly sampled but target color remained constant for each block of (10–200) trials. The red curve represents average performance from the first 5 trials following a color switch. The blue curve denotes average performance on a block of trials but excluding the first 5 trials after a color switch. (d) Task performance for monkey R from a previous study (Scerra et al., 2019). This subject ran a version of the CO task in which target locations were randomly sampled but target color did not change. Bin width is 50 ms for all curves. The gray trace in each panel shows the average tachometric curve obtained from all the trials considered.

Figure 2 — figure supplement 1.

Target color repetition affects perceptual accuracy in a consistent manner across subjects. (a–d) Task performance for monkey C. (e–h) Task performance for monkey N. (a, e) Individual subject tachometric curves denoting performance on the current trial conditioned on histories of preceding trials having the same target color (S, blue spectrum; 1–4 preceding trials) or different target color (D, red spectrum; 1–4 preceding trials). Average performance is shown in gray. The vertical gray shade represents the −29 ms shift used to align the data from monkey N with those from monkey C; it represents the centerpoints of the average tachometric curve of monkey N before (right edge of the shade) and after the shift (left edge of the shade). (b, f) Choice accuracies in short-PT trials (PT < 100 ms, floor). Error bars represent 95% CIs. Gray vertical lines denote values for the average tachometric curves. (c, g) Choice accuracies in long-PT trials (PT > 150 ms, ceiling). Error bars represent 95% CIs. Gray vertical lines denote values for the average tachometric curves. (d, h) Average RT ± 1 SEM for each history condition. The gray vertical lines denote the average RTs across all trials included in the analysis. Dark bars in h depict the aligned RT of monkey N shifted by −29 ms.

Figure 2 — figure supplement 2.

Target color repetition affects decision accuracy in a consistent manner across colors. (a) Tachometric curves denoting performance on green-target trials (see target array inset) conditioned on histories of preceding trials having the same target color (blue spectrum; 1–4 preceding green trials) or a different target color (red spectrum; 1–4 preceding red trials). (b) Choice accuracy in short-PT trials (PT < 100 ms, floor) conditioned on color history. Error bars represent 95% CIs across trials. Gray vertical line denotes value for the average tachometric curve. (c) Choice accuracy in long-PT trials (PT > 150 ms, ceiling) conditioned on color history. Error bars represent 95% CIs across trials. Gray vertical line denotes value for the average tachometric curve. (d) Average RT ± 1 SEM conditioned on color history. Gray vertical line denotes average RT across all trials included in the analysis. (e–h) As in a–d but for red targets among green distracters (see target array inset).