LIP responses to a popout stimulus are reduced if it is overtly ignored

Abstract

Bright objects capture our attention by virtue of 'popping out' from their surroundings. This correlates with strong responses in cortical areas thought to be important in attentional allocation. Previous studies have suggested that with the right mindset or training, humans can ignore popout stimuli. We studied the activity of neurons in monkey lateral intraparietal area while monkeys performed a visual search task. The monkeys were free to move their eyes, and a distractor, but never the search target, popped out. On trials in which the monkeys made a saccade directly to the search target, the popout distractor evoked a smaller response than the non-popout distractors. The intensity of the response to the popout correlated inversely with the monkeys' ability to ignore it. We suggest that this modulation corresponds to a top-down mechanism that the brain uses to adjust the parietal representation of salience.

Figure 1

Behavioral task. The monkeys began the task by grabbing two bars attached to the primate chair. A fixation point appeared, which the monkey had to look at for 1–1.75 s, after which it disappeared and was replaced by an eight-stimulus array positioned along an imaginary circle such that one member of the array was in the center of the receptive field of the neuron under study. One of the stimuli was the target and the remaining seven were distractors. In every trial, one of the distractors (a bright green stimulus) popped out. The monkeys had 3 s to report the orientation of the target by releasing one of the two bars. No constraints were imposed on the monkeys’ eye movements; they were not required to fixate the target before giving the response and were not penalized for not fixating the target.

Figure 2

Percentage of first saccades to the popout distractor before and during recording. In sessions before recording, blocks in which the popout was the target were occasionally presented. Left, data from these sessions, but only from blocks in which the popout was always a distractor. Right, data from recording sessions, in which the popout was never the target. Error bars show s.e.m.

Figure 3

Responses to the target or distractors within the neuron’s receptive field. All data are from trials in which the monkey made the first saccade to the target and released the correct bar. (a) Responses of a single cell to the appearance of an array object in the receptive field, versus time from target onset. Dark gray trace, response to the target in the receptive field when the monkey made a saccade to the target. Black trace, response to a non-popout distractor in the receptive field when the monkey made a saccade to the target (located elsewhere). Light gray trace, response to the popout distractor in the receptive field when the monkey made a saccade to the target (located elsewhere). (b) Same data as in a, but aligned on saccade onset. (c,d) Population averages for monkey R aligned to array onset (c) or saccade onset (d). (e,f) As in c and d, but for monkey Z. Thickness of the traces shows s.e.m.

Figure 4

Response to popout and non-popout distractors in three epochs of the trial for each monkey. (a,b) The response of each cell to the non-popout distractor is plotted against the response of the same cell to the popout distractor in the first 40 ms after the latency. (c,d) The responses in a 50-ms epoch after the first response, plotted as in a. (e,f) The responses in the interval ± 25 ms around saccade onset, plotted as in a.

Figure 5

Cell-by-cell correlation of response suppression with saccade suppression. (a,b) Percentage of trials in which the first saccade was made to the popout distractor for each cell, versus the difference in the number of spikes between the responses (within the time epoch from 80 ms to 130 ms after array onset) to the non-popout and popout distractors for the cell recorded in that session.