Activity in V4 Reflects the Direction, But Not the Latency, of Saccades During Visual Search (original) (raw)

Activity in the Lateral Intraparietal Area Predicts the Goal and Latency of Saccades in a Free-Viewing Visual Search Task

Journal of Neuroscience, 2006

The purpose of saccadic eye movements is to facilitate vision, by placing the fovea on interesting objects in the environment. Eye movements are not made for reward, and they are rarely restricted. Despite this, most of our knowledge about the neural genesis of eye movements comes from experiments in which specific eye movements are rewarded or restricted. Such experiments have demonstrated that activity in the lateral intraparietal (LIP) area of the monkey correlates with the monkey's planning of a memory-guided saccade or deciding where, on the basis of motion information, to make a saccade. However, other experiments have shown that neural activity in LIP can easily be dissociated from the generation of saccadic eye movements, especially when sophisticated behavioral paradigms dissociate the monkey's locus of attention from the goal of an intended saccade. In this study, we trained monkeys to report the results of a visual search task by making a nontargeting hand movement. Once the task began, the monkeys were entirely free to move their eyes, and rewards were not contingent on the monkeys making specific eye movements. We found that neural activity in LIP predicted not only the goal of the monkey's saccades but also their saccadic latencies.

Neural Control of Visual Search by Frontal Eye Field: Effects of Unexpected Target Displacement on Visual Selection and Saccade Preparation

The dynamics of visual selection and saccade preparation by the frontal eye field was investigated in macaque monkeys performing a search-step task combining the classic double-step saccade task with visual search. Reward was earned for producing a saccade to a color singleton. On random trials the target and one distractor swapped locations before the saccade and monkeys were rewarded for shifting gaze to the new singleton location. A race model accounts for the probabilities and latencies of saccades to the initial and final singleton locations and provides a measure of the duration of a covert compensation process—target-step reaction time. When the target stepped out of a movement field, noncompensated saccades to the original location were produced when movement-related activity grew rapidly to a threshold. Compensated saccades to the final location were produced when the growth of the original movement-related activity was interrupted within target-step reaction time and was replaced by activation of other neurons producing the compensated saccade. When the target stepped into a receptive field, visual neurons selected the new target location regardless of the monkeys' response. When the target stepped out of a receptive field most visual neurons maintained the representation of the original target location, but a minority of visual neurons showed reduced activity. Chronometric analyses of the neural responses to the target step revealed that the modulation of visually responsive neurons and movement-related neurons occurred early enough to shift attention and saccade preparation from the old to the new target location. These findings indicate that visual activity in the frontal eye field signals the location of targets for orienting, whereas movement-related activity instantiates saccade preparation.

Dissociation of spatial attention and saccade preparation

Proceedings of the National Academy of Sciences, 2004

The goal of this experiment was to determine whether the allocation of attention necessarily requires saccade preparation. To dissociate the focus of attention from the endpoint of a saccade, macaque monkeys were trained to perform visual search for a uniquely colored rectangle and shift gaze either toward or opposite this color singleton according to its orientation. A vertical singleton cued a prosaccade, a horizontal singleton, an antisaccade. Saccade preparation was probed by measuring the direction of saccades evoked by intracortical microstimulation of the frontal eye fields at variable times after presentation of the search array. Eye movements evoked on prosaccade trials deviated progressively toward the singleton that was also the endpoint of the correct eye movement. However, eye movements evoked on antisaccade trials never deviated toward the singleton but only progressively toward the location opposite the singleton. This occurred even though previous work showed that on antisaccade trials most neurons in frontal eye fields initially select the singleton while attention is allocated to distinguish its shape. Thus, sensorimotor structures can covertly orient attention without preparing a saccade.

Monkey prefrontal neuronal activity coding the forthcoming saccade in an oculomotor delayed matching-to-sample task

Journal of neurophysiology, 1998

To determine the role of the dorsolateral prefrontal cortex (PFC) in the selection of memory-guided saccadic eye movements, we recorded the activities of PFC neurons while macaque monkeys performed an oculomotor delayed matching-to-sample task. The task was designed to dissociate motor factors from visual factors in the selection and retention of the direction of the forthcoming saccade during delay periods after the visual cue but before the GO signal was presented. While the monkey fixated on a central fixation spot (FX period, 1 s), a sample cue (1 of 4 geometric figures) and a matching cue composed of two geometric figures were presented in succession (SC and MC periods, respectively, 0.5 s) with a brief delay (D1 period, 1 or 1.5 s). After another delay (D2 period, 1.5 s), the monkey made a saccade (GO period, <0.5 s) toward one of four locations (the goal) that had been indicated by the combination of the sample and matching cues in the MC period. We recorded the activities...

Saccade selection in visual search: evidence for spatial frequency specific between-item interactions

Vision Research, 1999

We present two experiments in which subjects were required to make a saccade to a target amongst distractors. Targets were oriented Gabor patches. Analysis of errors, when subjects fail to make a saccade to the target, showed two interesting features. First, most error saccades were directed towards a distractor and not to the blank space between distractors. This suggests that although the location of the target may not be encoded correctly, the locations of the items in the display are encoded. Second, when the display items were all of the same spatial frequency, a long-range effect occurred whereby the likelihood of an error saccade in a specific direction decreased systematically as the distance from the target increases. This systematic influence of the target location extended over practically the whole display. The long-range effect appeared whenever all display items had the same spatial frequency and showed little dependence on the spatial frequency of the display items. However, when the items had different spatial frequencies the long-range effects were absent.

Neuronal activity in macaque supplementary eye field during planning of saccades in response to pattern and spatial cues

Journal of neurophysiology, 2000

The aim of this study was to determine whether neuronal activity in the macaque supplementary eye field (SEF) is influenced by the rule used for saccadic target selection. Two monkeys were trained to perform a variant of the memory-guided saccade task in which any of four visible dots (rightward, upward, leftward, and downward) could be the target. On each trial, the cue identifying the target was either a spot flashed in superimposition on the target (spatial condition) or a foveally presented digitized image associated with the target (pattern condition). Trials conforming to the two conditions were interleaved randomly. On recording from 439 SEF neurons, we found that two aspects of neuronal activity were influenced by the nature of the cue. 1) Activity reflecting the direction of the impending response developed more rapidly following spatial than following pattern cues. 2) Activity throughout the delay period tended to be higher following pattern than following spatial cues. We...

Chapter 10 Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior

2006

Neural activity in the lateral intraparietal area (LIP) has been associated with attention to a location in visual space, and with the intention to make saccadic eye movement. In this study we show that neurons in LIP respond to recently flashed task-irrelevant stimuli and saccade targets brought into the receptive field by a saccade, although they respond much to the same stimuli when they are stable in the environment. LIP neurons respond to the appearance of a flashed distractor even when a monkey is planning a memory-guided delayed saccade elsewhere. We then show that a monkey's attention, as defined by an increase in contrast sensitivity, is pinned to the goal of a memory-guided saccade throughout the delay period, unless a distractor appears, in which case attention transiently moves to the site of the distractor and then returns to the goal of the saccade. LIP neurons respond to both the saccade goal and the distractor, and this activity correlates with the monkey's locus of attention. In particular, the activity of LIP neurons predicts when attention migrates from the distractor back to the saccade goal. We suggest that the activity in LIP provides a salience map that is interpreted by the oculomotor system as a saccade goal when a saccade is appropriate, and simultaneously is used by the visual system to determine the locus of attention.

Saliency and Saccade Encoding in the Frontal Eye Field During Natural Scene Search

Cerebral cortex (New York, N.Y. : 1991), 2013

The frontal eye field (FEF) plays a central role in saccade selection and execution. Using artificial stimuli, many studies have shown that the activity of neurons in the FEF is affected by both visually salient stimuli in a neuron's receptive field and upcoming saccades in a certain direction. However, the extent to which visual and motor information is represented in the FEF in the context of the cluttered natural scenes we encounter during everyday life has not been explored. Here, we model the activities of neurons in the FEF, recorded while monkeys were searching natural scenes, using both visual and saccade information. We compare the contribution of bottom-up visual saliency (based on low-level features such as brightness, orientation, and color) and saccade direction. We find that, while saliency is correlated with the activities of some neurons, this relationship is ultimately driven by activities related to movement. Although bottom-up visual saliency contributes to the choice of saccade targets, it does not appear that FEF neurons actively encode the kind of saliency posited by popular saliency map theories. Instead, our results emphasize the FEF's role in the stages of saccade planning directly related to movement generation.