Predictive enhancement of saccade target features in the pre-saccadic center of gaze

AbstractHumans and other primates are equipped with a foveated visual system. As a consequence, we reorient our fovea to objects and targets in the visual field that are conspicuous or that we consider relevant or worth looking at. These reorientations are achieved by means of saccadic eye movements. Where we saccade to depends on various low-level factors such as a targets’ luminance but also crucially on high-level factors like the expected reward or a targets’ relevance for perception and subsequent behavior. Here, we review recent findings how the control of saccadic eye movements is influenced by higher-level cognitive processes. We first describe the pathways by which cognitive contributions can influence the neural oculomotor circuit. Second, we summarize what saccade parameters reveal about cognitive mechanisms, particularly saccade latencies, saccade kinematics and changes in saccade gain. Finally, we review findings on what renders a saccade target valuable, as reflected in oculomotor behavior. We emphasize that foveal vision of the target after the saccade can constitute an internal reward for the visual system and that this is reflected in oculomotor dynamics that serve to quickly and accurately provide detailed foveal vision of relevant targets in the visual field.

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Mislocalization of stationary and flashed bars after saccadic inward and outward adaptation of reactive saccades

Journal of Neurophysiology ◽

10.1152/jn.00877.2011 ◽

2012 ◽

Vol 107 (11) ◽

pp. 3062-3070 ◽

Cited By ~ 7

Author(s):

Fabian Schnier ◽

Markus Lappe

Keyword(s):

Saccade Target ◽

Saccade Amplitude ◽

Presentation Duration ◽

Target Presentation ◽

Adaptation Mechanisms ◽

Long Duration ◽

Neuronal Mechanisms ◽

The Difference ◽

Saccade Adaptation

Recent studies have shown that saccadic inward adaptation (i.e., the shortening of saccade amplitude) and saccadic outward adaptation (i.e., the lengthening of saccade amplitude) rely on partially different neuronal mechanisms. There is increasing evidence that these differences are based on differences at the target registration or planning stages since outward but not inward adaptation transfers to hand-pointing and perceptual localization of flashed targets. Furthermore, the transfer of reactive saccade adaptation to long-duration overlap and scanning saccades is stronger after saccadic outward adaptation than that after saccadic inward adaptation, suggesting that modulated target registration stages during outward adaptation are increasingly used in the execution of saccades when the saccade target is visually available for a longer time. The difference in target presentation duration between reactive and scanning saccades is also linked to a difference in perceptual localization of different targets. Flashed targets are mislocalized after inward adaptation of reactive and scanning saccades but targets that are presented for a longer time (stationary targets) are mislocalized stronger after scanning than after reactive saccades. This link between perceptual localization and adaptation specificity suggests that mislocalization of stationary bars should be higher after outward than that after inward adaptation of reactive saccades. In the present study we test this prediction. We show that the relative amount of mislocalization of stationary versus flashed bars is higher after outward than that after inward adaptation of reactive saccades. Furthermore, during fixation stationary and flashed bars were mislocalized after outward but not after inward adaptation. Thus, our results give further evidence for different adaptation mechanisms between inward and outward adaptation and harmonize some recent research.

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The Main Sequence of Human Optokinetic Afternystagmus (OKAN)

Journal of Neurophysiology ◽

10.1152/jn.00114.2009 ◽

2009 ◽

Vol 101 (6) ◽

pp. 2889-2897 ◽

Cited By ~ 3

Author(s):

Andre Kaminiarz ◽

Kerstin Königs ◽

Frank Bremmer

Keyword(s):

Neural Networks ◽

Eye Movements ◽

Main Sequence ◽

Critical Role ◽

Saccade Target ◽

Control Mechanisms ◽

Visually Guided ◽

Background Characteristics ◽

Optokinetic Afternystagmus

Different types of fast eye movements, including saccades and fast phases of optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN), are coded by only partially overlapping neural networks. This is a likely cause for the differences that have been reported for the dynamic parameters of fast eye movements. The dependence of two of these parameters—peak velocity and duration—on saccadic amplitude has been termed “main sequence.” The main sequence of OKAN fast phases has not yet been analyzed. These eye movements are unique in that they are generated by purely subcortical control mechanisms and that they occur in complete darkness. In this study, we recorded fast phases of OKAN and OKN as well as visually guided and spontaneous saccades under identical background conditions because background characteristics have been reported to influence the main sequence of saccades. Our data clearly show that fast phases of OKAN and OKN differ with respect to their main sequence. OKAN fast phases were characterized by their lower peak velocities and longer durations compared with those of OKN fast phases. Furthermore we found that the main sequence of spontaneous saccades depends heavily on background characteristics, with saccades in darkness being slower and lasting longer. On the contrary, the main sequence of visually guided saccades depended on background characteristics only very slightly. This implies that the existence of a visual saccade target largely cancels out the effect of background luminance. Our data underline the critical role of environmental conditions (light vs. darkness), behavioral tasks (e.g., spontaneous vs. visually guided), and the underlying neural networks for the exact spatiotemporal characteristics of fast eye movements.

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Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

Journal of Neurophysiology ◽

10.1152/jn.00323.2012 ◽

2012 ◽

Vol 108 (5) ◽

pp. 1392-1402 ◽

Cited By ~ 15

Author(s):

Elsie Premereur ◽

Wim Vanduffel ◽

Pieter R. Roelfsema ◽

Peter Janssen

Keyword(s):

Spatial Attention ◽

Field Potential ◽

Gamma Oscillations ◽

Oculomotor Control ◽

Saccade Target ◽

Frontal Eye Field ◽

Alpha Power ◽

Lateral Intraparietal Area ◽

Electrical Microstimulation ◽

Gamma Power

Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.

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Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward

Journal of Neurophysiology ◽

10.1152/jn.1989.61.4.814 ◽

1989 ◽

Vol 61 (4) ◽

pp. 814-832 ◽

Cited By ~ 269

Author(s):

O. Hikosaka ◽

M. Sakamoto ◽

S. Usui

Keyword(s):

Spatial Information ◽

Target Location ◽

Hand Movement ◽

Visual Fixation ◽

Saccade Target ◽

Tonic Activity ◽

Sustained Activity ◽

Neural Activities ◽

Reward Expectancy ◽

Mouth Movement

1. The present paper reports complex neural activities in the monkey caudate nucleus that precede and anticipate visual stimuli and reward in learned visuomotor paradigms. These activities were revealed typically in the delayed saccade task in which memory and anticipation were required. We classified these activities according to their relationships to the task. 2. Activity related to expectation of a cue (n = 46) preceded the presentation of a spot of light (target cue) that signified the future location of saccade target. When the target cue was delayed, the activity was prolonged accordingly. The same spot of light was preceded by no activity if it acted as a distracting stimulus. 3. The sustained activity (n = 80) was a tonic discharge starting after the target cue as if holding the spatial information. 4. The activity related to expectation of target (n = 109) preceded the appearance of the target whose location was cued previously. It started with or after a saccade to the cued target location and ended with the appearance of the target. The activity was greater when the target was expected to appear in the contralateral visual field. 5. The activity related to expectation of reward (n = 57) preceded a task-specific reward. It started with the appearance of the final target and ended with the reward. In most cases, the activity was nonselective for how the monkey obtained the reward, i.e., by visual fixation only, by a saccade, or by a hand movement. The activity was dependent partly on visual fixation. 6. A few neurons showed tonic activity selectively before lever release and are thus considered to be related to the preparation of hand movements. 7. The activity related to breaking fixation (n = 33) occurred phasically if the monkey broke fixation, aborting the trial. 8. Activity related to reward (n = 104) was a phasic discharge that occurred before or after a reward of water was delivered. The activity was not simply related to a specific movement involved in the reward-obtaining behavior (eye, hand, or mouth movement). 9. Fixation-related activity (n = 72) was tonic activity continuing as long as the monkey attentively fixated a spot of light. It was dependent on reward expectancy in most cases. 10. The present results, together with those in the preceding papers, indicate that the activities of individual caudate neurons--sensory, motor, or cognitive--are dependent on specific contexts of learned behavior.(ABSTRACT TRUNCATED AT 400 WORDS)

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Salience by Competitive and Recurrent Interactions: Bridging Neural Spiking and Computation

10.31234/osf.io/rkh8g ◽

2021 ◽

Author(s):

Gregory Edward Cox ◽

Thomas Palmeri ◽

Gordon D. Logan ◽

Philip L. Smith ◽

Jeffrey Schall

Keyword(s):

Decision Making ◽

Response Times ◽

Target Selection ◽

Interaction Model ◽

Saccade Target ◽

Frontal Eye Field ◽

Visual Neurons ◽

Discharge Rates ◽

Neural Spiking ◽

Eye Field

Decisions about where to move the eyes depend on neurons in Frontal Eye Field (FEF). Movement neurons in FEF accumulate salience evidence derived from FEF visual neurons to select the location of a saccade target among distractors. How visual neurons achieve this salience representation is unknown. We present a neuro-computational model of target selection called Salience by Competitive and Recurrent Interactions (SCRI), based on the Competitive Interaction model of attentional selection and decision making (Smith & Sewell, 2013). SCRI selects targets by synthesizing localization and identification information to yield a dynamically evolving representation of salience across the visual field. SCRI accounts for neural spiking of individual FEF visual neurons, explaining idiosyncratic differences in neural dynamics with specific parameters. Many visual neurons resolve the competition between search items through feedforward inhibition between signals representing different search items, some also require lateral inhibition, and many act as recurrent gates to modulate the incoming flow of information about stimulus identity. SCRI was tested further by using simulated spiking representations of visual salience as input to the Gated Accumulator Model of FEF movement neurons (Purcell et al., 2010; Purcell, Schall, Logan, & Palmeri, 2012). Predicted saccade response times fit those observed for search arrays of different set size and different target-distractor similarity, and accumulator trajectories replicated movement neuron discharge rates. These findings offer new insights into visual decision making through converging neuro-computational constraints and provide a novel computational account of the diversity of FEF visual neurons.

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Modulations of foveal vision associated with microsaccade preparation

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1919832117 ◽

2020 ◽

Vol 117 (20) ◽

pp. 11178-11183

Author(s):

Natalya Shelchkova ◽

Martina Poletti

Keyword(s):

Eye Movements ◽

Visual Discrimination ◽

Target Location ◽

Onset Time ◽

Spatial Vision ◽

Saccade Target ◽

Foveal Vision ◽

Movement Onset ◽

High Acuity ◽

Gaze Position

It is known that attention shifts prior to a saccade to start processing the saccade target before it lands in the foveola, the high-resolution region of the retina. Yet, once the target is foveated, microsaccades, tiny saccades maintaining the fixated object within the fovea, continue to occur. What is the link between these eye movements and attention? There is growing evidence that these eye movements are associated with covert shifts of attention in the visual periphery, when the attended stimuli are presented far from the center of gaze. Yet, microsaccades are primarily used to explore complex foveal stimuli and to optimize fine spatial vision in the foveola, suggesting that the influences of microsaccades on attention may predominantly impact vision at this scale. To address this question we tracked gaze position with high precision and briefly presented high-acuity stimuli at predefined foveal locations right before microsaccade execution. Our results show that visual discrimination changes prior to microsaccade onset. An enhancement occurs at the microsaccade target location. This modulation is highly selective and it is coupled with a drastic impairment at the opposite foveal location, just a few arcminutes away. This effect is strongest when stimuli are presented closer to the eye movement onset time. These findings reveal that the link between attention and microsaccades is deeper than previously thought, exerting its strongest effects within the foveola. As a result, during fixation, foveal vision is constantly being reshaped both in space and in time with the occurrence of microsaccades.

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Shape Selectivity in Primate Frontal Eye Field

Journal of Neurophysiology ◽

10.1152/jn.01188.2007 ◽

2008 ◽

Vol 100 (2) ◽

pp. 796-814 ◽

Cited By ~ 38

Author(s):

Xinmiao Peng ◽

Margaret E. Sereno ◽

Amanda K. Silva ◽

Sidney R. Lehky ◽

Anne B. Sereno

Keyword(s):

Functional Organization ◽

Target Selection ◽

Visual Stimuli ◽

Shape Selectivity ◽

Saccade Target ◽

Frontal Eye Field ◽

Gaze Shift ◽

Match To Sample ◽

Neurophysiological Studies ◽

Eye Field

Previous neurophysiological studies of the frontal eye field (FEF) in monkeys have focused on its role in saccade target selection and gaze shift control. It has been argued that FEF neurons indicate the locations of behaviorally significant visual stimuli and are not inherently sensitive to specific features of the visual stimuli per se. Here, for the first time, we directly examined single cell responses to simple, two-dimensional shapes and found that shape selectivity exists in a substantial number of FEF cells during a passive fixation task or during the sample, delay (memory), and eye movement periods in a delayed match to sample (DMTS) task. Our data demonstrate that FEF neurons show sensory and mnemonic selectivity for stimulus shape features whether or not they are behaviorally significant for the task at hand. We also investigated the extent and localization of activation in the FEF using a variety of shape stimuli defined by static or dynamic cues employing functional magentic resonance imaging (fMRI) in anesthetized and paralyzed monkeys. Our fMRI results support the electrophysiological findings by showing significant FEF activation for a variety of shape stimuli and cues in the absence of attentional and motor processing. This shape selectivity in FEF is comparable to previous reports in the ventral pathway, inviting a reconsideration of the functional organization of the visual system.

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Relation Between the Metrics of the Presaccadic Attention Shift and of the Saccade Before and After Saccadic Adaptation

Journal of Neurophysiology ◽

10.1152/jn.2000.84.4.1809 ◽

2000 ◽

Vol 84 (4) ◽

pp. 1809-1813 ◽

Cited By ~ 19

Author(s):

J. Ditterich ◽

T. Eggert ◽

A. Straube

Keyword(s):

Hierarchical Level ◽

Saccade Target ◽

Eye Position ◽

Attention Shift ◽

Short Term ◽

Saccadic Adaptation ◽

Attention Focus ◽

Before And After ◽

Saccade Size ◽

Saccade Programming

A shift of the visual attention focus is known to precede saccades. However, how the metrics of both this presaccadic attention shift and the saccade are coupled is still unclear. We altered the saccade size by short-term saccadic adaptation to determine whether the attention focus would still be shifted to the location of the saccade target or to the modified postsaccadic eye position. The results showed that saccadic adaptation had no influence on the presaccadic attention shift. Thus either different processes determine the metrics of the attention shift and of the saccade or saccadic adaptation causes only modifications on a lower hierarchical level of saccade programming, thereby not influencing the metrics of the attention shift.

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