Elsevier

Consciousness and Cognition

Volume 19, Issue 4, December 2010, Pages 861-871
Consciousness and Cognition

Awareness of the saccade goal in oculomotor selection: Your eyes go before you know

https://doi.org/10.1016/j.concog.2010.04.001Get rights and content

Abstract

The aim of the present study was to investigate how saccadic selection relates to people’s awareness of the saliency and identity of a saccade goal. Observers were instructed to make an eye movement to either the most salient line segment (Experiment 1) or the only right-tilted element (Experiment 2) in a visual search display. The display was masked contingent on the first eye movement and after each trial observers indicated whether or not they had correctly selected the target. Whereas people’s awareness concerning the saliency of the saccade goal was generally low, their awareness concerning the identity was high. Observers’ awareness of the saccade goal was not related to saccadic performance. Whereas saccadic selection consistently varied as a function of saccade latency, people’s awareness concerning the saliency or identity of the saccade goal did not. The results suggest that saccadic selection is primarily driven by subconscious processes.

Introduction

Saccadic movements or saccades are rapid changes in eye position that occur three or four times each second. The purpose of saccades is to bring information to the central area of the retina called the fovea where spatial acuity is best. During the more or less stationary periods between saccades, called fixations, information is acquired for processing and the landing point of the next saccade may be determined. Whereas it is generally acknowledged that saccadic programming, for the most part, operates below the level of conscious awareness (Findlay and Gilchrist, 2003, Haggard, 2005, Mokler and Fischer, 1999, Westheimer and Mitchell, 1969), the role of awareness in the saccadic selection of information is less determined. The aim of the present study was to investigate the extent to which observers’ awareness concerning a saccade goal is related to saccadic selection performance.

It is possible to make a distinction between at least three different views with respect to this issue. First, it may be the case that observers are at all times aware of the information that is overtly selected for closer inspection. In other words, observers are aware of the property of the saccade goal that is selected. For example, if an observer selects a saccade goal on the basis of its color, the observer will be aware of this color; and likewise for other properties such as orientation, stimulus-saliency and location. The idea here is that objects or locations selected for foveal viewing reach observer’s awareness via the attentional system. This proposal is based on the idea that attention is tightly related to the saccadic system (Belopolsky et al., 2008, Deubel and Schneider, 1996, Klein, 1980, Klein and Pontefract, 1994, Kowler et al., 1995, Rizzolatti et al., 1987, Sheliga et al., 1995). Accordingly, many theories assume that a shift in covert attention precedes the eye movement to a location (Deubel and Schneider, 1996, Henderson, 1992, Hoffman and Subramaniam, 1995, Kowler et al., 1995, Schneider and Deubel, 1995). Although the relationship between attention and awareness is still a matter of debate, attention has been proposed to act as a requisite for awareness (e.g., Posner, 1994). For example, Lamme, 2003, Lamme, 2004 has argued that attention may act as a gate towards a representation that can be consciously reported. Given the relation between attention and eye movements, and between attention and awareness, attention may provide the critical link between awareness and eye movements. If attention precedes the eyes to a selected location and if attention acts as a requisite for awareness, observers should always be aware of the information they select for foveal viewing.

Second, it may be that awareness of the saccade goal is related to the response latency of the saccade. Observers may not be aware of the information that drives a response when the response is executed shortly following display presentation. However, as times passes and information about the goal location accrues, observers may be become increasingly aware of this information and responses may become increasingly based on this conscious information. Accordingly, observers’ awareness may develop over time and be related to whether responses were triggered earlier or later in the stream of processing (Johnson, Van Beers, & Haggard, 2002). This distinction between short-latency and long-latency responses is corroborated by differences in the time-course between stimulus- and goal-driven mechanisms of selection. Whereas early selection is primarily automatic and determined by visually salient properties of a display, late selection tends to be more volitional and controlled by the goals and intentions of the observer (Donk and van Zoest, 2008, van Zoest and Donk, 2005, van Zoest and Donk, 2006, van Zoest and Donk, 2008, van Zoest et al., 2004). With regards to observers’ awareness, it may be the case that observers are unaware of the saccade goal when they make fast stimulus-driven eye movements, yet are aware of the saccade goal when they make slow goal-driven eye movement (however, see Sumner & Husain, 2008). Various studies demonstrate that people do not have much conscious recollection concerning the saccade goal when eye movements are stimulus-driven. Specifically, observers may not be aware of the fact that they make eye movements directed to salient objects in the visual field (Belopolsky et al., 2008, Kramer et al., 2000, Theeuwes et al., 1998, Zhaoping, 2008). Experimental support for the idea that observers are aware of the saccade goal in goal-driven selection is less readily available. However, this seems to be related to the naturalness of the idea rather than to the lack of evidence. Processes that underlie visual awareness are very similar to those that regulate voluntary movements (e.g., Hallett, 2007). As a consequence, it is often assumed that per definition, goal-driven selection is accompanied by awareness of the saccade goal. Thus, according to this second view, observers’ awareness depends on saccade latency and may in part be driven by differences in the time-course of stimulus-driven and goal-driven control of selection.

A third view on the relationship posits that people are unaware of the information that guides saccadic selection. In line with this view, is evidence showing that observers are unaware of the location of a saccade goal even though they were making a voluntary eye movement. Such findings are primarily derived from studies using a ‘double-step paradigm’ (Bridgeman et al., 1975, Bridgeman et al., 1981, Bridgeman et al., 1979, Castiello et al., 1991, Johnson and Haggard, 2005, Prablanc and Martin, 1992, Pélisson et al., 1986). In this task, participants are required to make a saccade to a visual target. However, during the saccadic eye movement the visual target may unpredictably shift a small distance. The results typically show that even though observers fail to detect the shift of the visual target, participants were still able to saccade or point correctly to the center of the target (Bridgeman et al., 1975, Bridgeman et al., 1979). This work demonstrates that observers are not always aware of the visual information that guides the oculomotor system (see also, Deubel et al., 1999, Koch and Tsuchiya, 2007). According to the third view, this may be the rule rather than the exception. Moreover, this may not only apply to information concerning the location of a saccade goal but also apply to other properties of the saccade goal, such as the color, orientation and saliency.

To briefly summarize, there are different perspectives regarding the relationship between awareness of the saccade goal and saccadic selection performance. However, little work has been conducted to investigate the differences between these views systematically. The aim of the present study was to investigate the extent to which observers were aware of the saccade goal that is selected for further processing. More specifically, in the present study we investigated whether observers were aware of the saliency (Experiment 1) and the orientation (Experiment 2) of a saccade goal and investigated the relationship between observers’ awareness and oculomotor performance. In Experiment 1 participants were instructed to select the most visually salient element in the display. In Experiment 2, participants were instructed to search for a pre-specified identity, a line oriented to the right. Eye movements were monitored and the proportion of correct eye movements to the target was analyzed as a function of saccade latency. Contingent on the first eye movement, the search display was masked. Participants’ awareness of the saccade goal was tested after each trial. In Experiment 1, participants indicated whether or not they correctly moved their eyes to the most salient element. In Experiment 2, participants indicated whether or not they correctly moved their eyes to the right-tilted element. Participants’ report indicating whether an eye movement was correctly directed to the target was used to calculate the sensitivity index d-prime. d-Prime was also analyzed as a function of saccade latency to investigate whether observers’ awareness varied as a function of the time after the presentation of the stimulus display. Note that with saccade goal we refer to the information at the landing position of the first eye movement, irrespective of whether the correct target or incorrect distractor was selected.

Based on the three perspectives discussed above we can formulate three predictions. If participants are fully aware of the information they select for foveal viewing (view I), we predict that observer’s overall awareness of the saccade goal will be high. Furthermore, this high level-of-awareness should characterize saccadic selection independent of whether observers were fast or slow to select the saccade goal. If observers’ awareness depends on the saccade latency (view II), we predict that the degree of awareness will depend on whether observers were fast or slow to make an eye movement. In this case, awareness is predicted to increase with saccade latency. Short-latency eye movements that are primarily driven by stimulus-driven control should occur with little awareness of the saccade goal. As saccade latency increases and selection becomes more goal-driven, the level-of-awareness of the saccade goal is predicted to become higher. If saccadic selection occurs completely outside awareness (view III), we predict that observers will be scarcely aware of the saccade goal. Furthermore, this low level-of-awareness should not depend on saccade latency.

Section snippets

Method

Experiment 1 investigated the extent to which observers’ awareness of the relative saliency of the saccade goal is related to saccadic target selection. Observers were presented with displays containing multiple homogenously oriented background lines and two singletons, each defined by a different orientation-contrast relative to the background lines. The difference between the singleton and the background elements was either 20° or 70°. Participants were given the instruction to make an eye

Method

Participants were instructed to make an eye movement to the orientation singleton that was tilted to the right. The right-tilted orientation singleton was either a salient or a non-salient singleton in the display. Note that in the latter case there is a conflict between stimulus-driven and goal-driven influences. Similar to Experiment 1, the search display was masked contingent to the eye movement, such that participants viewed a mask when their eyes landed on the saccade goal. Following each

General discussion

In two experiments, we investigated the extent to which observers’ awareness of the saccade goal was related to saccadic selection performance. Participants were required to saccade to the either the most salient line element (Experiment 1) or the line element that was tilted to the right (Experiment 2) in a search display consisting of two singletons and multiple homogenously oriented background lines. The search display was masked contingent on the start of the first saccade such that the

Acknowledgement

WvZ was supported by a grant from the Netherlands Organization for Scientific Research.

References (64)

  • V.A. Lamme

    Why visual attention and awareness are different

    Trends in Cognitive Sciences

    (2003)
  • V.A. Lamme

    Separate neural definitions of visual consciousness and visual attention; a case for phenomenal awareness

    Neural Networks

    (2004)
  • J.A. Mazer et al.

    Goal-related activity in V4 during free viewing visual search. Evidence for a ventral stream visual salience map

    Neuron

    (2003)
  • G. Rizzolatti et al.

    Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention

    Neuropsychologia

    (1987)
  • G. Westheimer et al.

    The sensory stimulus for disjunctive eye movements

    Vision Research

    (1969)
  • R.A. Andersen

    Visual and eye movement functions of the posterior parietal cortex

    Annual Review of Neuroscience

    (1989)
  • A.V. Belopolsky et al.

    The role of awareness in processing of oculomotor capture: Evidence from event-related potentials

    Journal of Cognitive Neuroscience

    (2008)
  • B. Bridgeman et al.

    Segregation of cognitive and motor aspects of visual function using induced motion

    Perception & Psychophysics

    (1981)
  • B. Bridgeman et al.

    Relation between cognitive and motor-oriented systems of visual position perception

    Journal of Experimental Psychology: Human Perception and Performance

    (1979)
  • U. Castiello et al.

    Temporal dissociation of motor responses and subjective awareness. A study in normal subjects

    Brain

    (1991)
  • P. Dassonville et al.

    Perception, action, and roelofs effect: A mere illusion of dissociation

    PLoS Biology

    (2004)
  • D.D. de Grave et al.

    Why are saccades influenced by the Brentano illusion?

    Experimental Brain Research

    (2006)
  • M. Desmurget et al.

    Movement intention after parietal cortex stimulation in humans

    Science

    (2009)
  • C. de’Sperati et al.

    Blind saccades: An asynchrony between seeing and looking

    Journal of Neuroscience

    (2008)
  • H. Deubel et al.

    The subjective direction of gaze shifts long before the saccade

  • M. Donk et al.

    Salience is only briefly represented: Evidence from probe-detection performance

    Journal of Experimental Psychology: Human Perception and Performance

    (2010)
  • M. Donk et al.

    Effects of salience are short-lived

    Psychological Science

    (2008)
  • M.P. Eckstein et al.

    Similar neural representations of the target for saccades and perception during search

    Journal of Neuroscience

    (2007)
  • T. Endrass et al.

    ERP correlates of conscious error recognition: Aware and unaware errors in an antisaccade task

    European Journal of Neuroscience

    (2007)
  • J.M. Findlay et al.

    Active vision

    (2003)
  • V.H. Franz et al.

    Grasping visual illusions: Consistent data and no dissociation

    Cognitive Neuropsychology

    (2008)
  • M.E. Goldberg et al.

    The role of the lateral intraparietal area of the monkey in the generation of saccades and visuospatial attention

    Annals of the New York Academy of Sciences

    (2002)
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