LIP activity in the interstimulus interval of a change detection task biases the behavioral response

Abstract

When looking around at the world, we can only attend to a limited number of locations. The lateral intraparietal area (LIP) is thought to play a role in guiding both covert attention and eye movements. In this study, we tested the involvement of LIP in both mechanisms with a change detection task. In the task, animals had to indicate whether an element changed during a blank in the trial by making a saccade to it. If no element changed, they had to maintain fixation. We examine how the animal's behavior is biased based on LIP activity prior to the presentation of the stimulus the animal must respond to. When the activity was high, the animal was more likely to make an eye movement toward the stimulus, even if there was no change; when the activity was low, the animal either had a slower reaction time or maintained fixation, even if a change occurred. We conclude that LIP activity is involved in both covert and overt attention, but when decisions about eye movements are to be made, this role takes precedence over guiding covert attention.

Keywords: attention; eye movement; lateral intraparietal area.

Fig. 1.

Change blindness task. After animals fixated a central spot, 1, 2, 4, or 8 oriented bars were flashed in a circular array around the fixation point, with 1 bar placed in the center of the response field (RF) of the neuron. The animals had to keep fixation during the presentation of this array (array 1). After a gap of 50–300 ms, the oriented bars reappeared (array 2), but 1 of the bars could have changed orientation by rotating 90° (change trial), in which case the animals had 1 s to make an eye movement to the rotated bar to be rewarded. If no rotation occurred, the animals had to keep fixation for 1 s to be rewarded (no-change trial).

Fig. 2.

Performance in the change detection task. A: mean (±SE) % correct is plotted as a function of the number of stimuli in the array (set size) for the individual animals. B: mean (±SE) % of hit trials is plotted as a function of the number of stimuli in the array. C: mean (±SE) % of correct rejection (CR) trials is plotted as a function of the number of stimuli in the array. Note that % of false alarm trials is equal to 100 − % of correct rejection trials.

Fig. 3.

Response to array 2 in the change detection task. A–C: mean population responses across both orientations from neurons with gaps of ≥100 ms in hit trials and in correct rejection trials plotted as a function of time from array 2 onset for set size 1 (A), set size 2 (B), and set size 4 (C). Vertical dashed lines show start and end of analysis epochs: 50–150 ms (dark gray column) and 150–300 ms (light gray column). Arrows indicate median reaction time (RT) for each condition. D–F: mean response 50–150 ms after the onset of array 2 in hit trials plotted against mean response from the same window in correct rejection trials for set size 1 (D; P = 1.5 × 10⁻¹¹, Wilcoxon signed-rank test), set size 2 (E; P = 7.1 × 10⁻¹³), and set size 4 (F; P = 1.4 × 10⁻¹⁰). G–I: mean response 150–300 ms after the onset of array 2 in hit trials plotted against mean response from the same window in correct rejection trials for set size 1 (G; P = 4.6 × 10⁻¹³, Wilcoxon signed-rank test), set size 2 (H; P = 4.1 × 10⁻¹⁷), and set size 4 (I; P = 6.9 × 10⁻¹³).

Fig. 4.

Relationship between the response during the interstimulus interval and behavior for set size 1. A: mean population responses in hit, correct rejection, and miss trials plotted as a function of time from array 2 onset. B: mean response during the interstimulus interval (ISI; gray bar in A) in hit trials plotted against mean response in miss trials (P = 0.0038, Wilcoxon signed-rank test). C: mean population responses in hit, correct rejection, and false alarm (FA) trials plotted as a function of time from array 2 onset. D: mean response during the interstimulus interval in false alarm trials plotted against mean response in correct rejection trials (P = 0.011). E: mean population responses in short-reaction time hit trials and long-reaction time hit trials plotted as a function of time from array 2 onset. F: mean response during the interstimulus interval in hit trials with short reaction times plotted against mean response in hit trials with long reaction times (P = 3.1 × 10⁻⁵, Wilcoxon signed-rank test). In B, D, and F, histograms show the distribution of differences in responses within single neurons across the 2 conditions.

Fig. 5.

Relationship between the response during the interstimulus interval and behavior on change trials for set sizes 2 and 4. A and C: mean population responses in hit, correct rejection, and miss trials plotted as a function of time from array 2 onset for set size 2 (A) and set size 4 (C). B and D: mean response during the interstimulus interval in hit trials plotted against mean response in miss trials for set size 2 (B; P = 0.032, 1-tailed Wilcoxon signed-rank test) and set size 4 (D; P = 0.0013). Histograms show the distribution of differences in responses within single neurons across the 2 conditions.

Fig. 6.

Relationship between the response during the interstimulus interval and behavior on no-change trials for set sizes 2 and 4. A and C: mean population responses in hit, correct rejection, and false alarm trials plotted as a function of time from array 2 onset for set size 2 (A) and set size 4 (C). B and D: mean response during the interstimulus interval in false alarm trials plotted against mean response in correct rejection trials for set size 2 (B; P = 0.015, 1-tailed Wilcoxon signed-rank test) and set size 4 (D; P = 0.031). Histograms show distribution of differences in responses within single neurons across the 2 conditions.

Fig. 7.

Relationship between the response during the interstimulus interval and the animals' reaction times for set size 2 and set size 4. A: mean population responses in short-reaction time hit trials and long-reaction time hit trials plotted as a function of time from array 2 onset for set size 2. B: mean response during the interstimulus interval in trials with short reaction times plotted against mean response in correct trials with long reaction times for set size 2 (P = 0.00010, 1-tailed Wilcoxon signed-rank test). C: mean population responses in short-reaction time hit trials and long-reaction time hit trials plotted as a function of time from array 2 onset for set size 4. D: mean response during the interstimulus interval in trials with short reaction times plotted against the mean response in correct trials with long reaction times for set size 4 (P = 0.060). In B and D, histograms show distribution of differences in responses within single neurons across the 2 conditions.

Fig. 8.

Responses to array 2 aligned by saccade onset: mean population responses in hit, correct rejection, and false alarm trials plotted as a function of time from saccade onset for set size 1 (A), set size 2 (B), and set size 4 (C). For correct rejection trials, data were aligned by the median saccadic latency from hit trials. Data in all traces come only from cells in which there were >5 false alarm trials. Gray columns show analysis period from which the perisaccadic response was calculated.