A saccade usually lasts less than 40 ms and redirects the center of sight in the visual field. Saccades occur several times per second, and each intervening period of fixation lasts several hundred milliseconds. The Russian psychologist Alfred Yarbus was the first to show that the pattern of saccades made by a human looking at a picture reflected the cognitive purpose of vision. He found that saccades were not directed equally to all parts of a scene. Areas of apparent interest were fixated most frequently, whereas background objects were ignored. For example, the faces of people were fixated repeatedly (Figure 29–2).
Eye movements during vision.
A subject viewed this painting (An Unexpected Visitor by Ilya Repin) for several minutes, making saccades to selected fixation points—primarily faces—that presumably were of most interest. Lines indicate saccades, and spots indicate points at which the eyes fixated. (Reproduced, with permission, from Yarbus 1967.)
The image on the fovea shifts with each saccade, yet we perceive a stable visual world. How does that come about? One possibility is that the brain creates a representation of the entire visual scene from a series of visual fixations across the scene and that what we see is this summed representation of the visual world. If that were so, we should have detailed knowledge of the entire visual scene at any given instant.
A series of experiments on change blindness showed that this is not the case. These experiments involved changing a picture during the brief time when the viewer made a saccade from one part of the scene to another. If there were a relatively complete internal representation of the scene before the saccade, then any substantial change made during the saccade should have been recognized. But even a large change frequently went unrecognized. This change blindness occurred even when there were no actual eye movements, as when two pictures were shown in succession with only a brief blank between them to simulate the effect of an eye movement (Figure 29–3).
In this example one picture is presented followed by a blank for 80 ms, followed by the second picture, another blank, and a repeat of the cycle. The subject is asked to report what changed in the scene. There is a substantial and, once perceived, obvious change between the two pictures. It takes multiple repetitions for most observers to detect the difference. (Reproduced, with permission, from Ronald Rensink.)
The results of the change-blindness experiments are inconsistent with the hypothesis that we are continually updating a complete representation of the visual field from second to second. Instead we seem to pay attention to only certain fragments of the scene. This selective visual attention relies on the saccades that bring the images of desired parts of the visual field onto the fovea.
Attention Selects Objects for Further Visual Examination
In the 19th century William James described attention as "the taking possession by the mind in clear and vivid form, of one out of what seem several simultaneously possible objects or trains of thought. It implies withdrawal from some things in order to deal effectively with others." James went on to describe two kinds of attention: "It is either passive, reflex, non-voluntary, effortless or active and voluntary. In passive immediate sensorial attention the stimulus is a sense-impression, either very intense, voluminous, or sudden … big things, bright things, moving things … blood."
More recently these two kinds of attention have been termed involuntary (exogenous) and voluntary (endogenous) attention, or bottom-up and top-down attention. Your attention to this page as you read it is an example of voluntary attention. If a bright light suddenly flashed, your attention would probably be pulled away involuntarily from the page.
Voluntary attention is closely linked to saccades because the fovea has a much denser array of cones than the peripheral retina (see Figure 26–1), and this permits a finer-grain analysis of objects than is possible with peripheral vision.
Attention, both voluntary and involuntary, has several measurable effects on human visual performance: It shortens reaction time and makes perception more sensitive. This increased sensitivity includes the abilities to detect objects at a lower contrast and ignore distracters close to an object. The abrupt appearance of a behaviorally irrelevant cue such as a light flash reduces the reaction time to a test stimulus presented 300 ms later in the same place, but increases reaction time when the test stimulus appears at a different place. The light flash involuntarily draws attention to itself, and attention to that location is maintained for a brief period, thus accelerating the visual response to the later test stimulus at the location. Similarly, if a subject plans a saccade to a particular part of the visual field, the contrast threshold at which any object there can be seen is lowered by 50%. The saccade, under voluntary control, draws attention to its goal.
Activity in the Parietal Lobe Correlates with Attention Paid to Objects
Clinical studies have long implicated the parietal lobe in the process of visual attention. Patients with lesions of the right parietal lobe have normal visual fields when their visual perception is studied with a single stimulus in an uncomplicated visual world. However, when presented with a more complicated world, with objects in the right (ipsilateral) and left (contralateral) visual hemifields, they tend to report more of what lies in the right visual hemifield.
This deficit, known as neglect syndrome (see Chapter 17), arises because attention is focused on the visual hemifield ipsilateral to the lesion. Even when patients are presented with only two stimuli, one in each field, they report seeing only the stimulus in the ipsilateral hemifield. They do not have the ability to focus attention in the hemifield contralateral to the lesion, and as a result they may not see everything in that hemifield, even though the sensory pathway from the eye to the striate and prestriate cortex is intact.
This neglect of the contralateral visual hemifield extends to the neglect of the contralateral half of individual objects. Patients with right parietal deficits often have difficulty reproducing drawings. When asked to draw a clock, for example, they may force all of the numbers into the right side of the face (see Figure 17–11), or when asked to draw a candlestick they may draw only its right side (Figure 29–4).
Drawing of a candlestick by a patient with a right parietal lesion.
The patient neglects the left side of the candlestick, drawing only its right half. (Reproduced, with permission, from Peter Halligan.)
The process of attentional selection is evident at the level of single parietal neurons in the monkey. The responses of neurons in the lateral intraparietal area to a visual stimulus depend not only on the physical properties of the stimulus but also on how the monkey behaves toward it. When a monkey fixates a spot, a stimulus in the neuron's receptive field evokes a moderate response. When the animal must attend to the same stimulus, the stimulus evokes a greater response, often by a factor of two. Conditions that evoke both involuntary and voluntary attention—the abrupt onset of a visual stimulus in the receptive field or the planning of a saccade to the receptive field of the neuron—evoke still greater responses (Box 29–1).
Box 29–1 The Effect of Behavioral Significance on Neuronal Responses
The responses of neurons in the lateral intraparietal area to visual stimuli vary with the behavioral significance of stimuli as well as the physical characteristics of the stimuli. This can be demonstrated by recording from neurons while a monkey makes eye movements across a stable array.
Stable objects in the visual world are rarely the objects of attention. In the lateral intraparietal area, as in most other visual centers of the brain, neuronal receptive fields are retinoptic, that is, they are defined relative to the center of gaze. As a monkey scans the visual field, fixed objects enter and leave the receptive fields of neurons with every eye movement without attracting the animal's attention (Figure 29–5).
The abrupt appearance of a visual stimulus can evoke involuntary attention, however. When a light flashes in the receptive field of a lateral intraparietal neuron, that cell responds briskly (Figure 29–6A). In contrast, a stable, task-irrelevant stimulus evokes little response when eye movements bring it into the neuron's receptive field (Figure 29–6B).
When the stimulus appears abruptly outside the receptive field, a saccade brings the attention-commanding stimulus into the receptive field, evoking a large response from the neuron (Figure 29–6C). When the monkey makes the saccade, the objects in the visual field are identical in both cases. However, the stable stimulus is presumably unattended, whereas the light flash evokes attention and provokes a much larger response. Stable objects can evoke enhanced responses when they become relevant to the animal's current behavior.
In the experiment of Figure 29–7 the monkey begins by fixating one of several images outside the receptive field. A cue appears, also outside the receptive field, that tells the monkey which image it should fixate after a saccade to the center of the array of images. If this second target is already in the receptive field the stimulus evokes a large response. If it is not, the stimulus evokes little response when the saccade brings it into the receptive field. Thus attention modulates the activity of neurons in the lateral intraparietal cortex (LIP) regardless of how that attention is evoked.
Exploring a stable array of objects.
The monkey views a screen with a number of objects, which remain in place throughout the experiment. The monkey's gaze can be positioned so that none of the objects are included in the receptive field of a neuron (left), or the monkey can make a saccade that brings one of the objects into the receptive field (right). (Reproduced, with permission, from Kusunoki, Gottlieb, and Goldberg 2000.)
A neuron in the lateral intraparietal area fires only in response to salient stimuli.
In each panel neuronal activity along with horizontal (H) and vertical (V) eye positions are plotted against time.
A. A stimulus flashes in the receptive field while the monkey fixates.
B. The monkey makes a saccade that brings a stable, task-irrelevant stimulus into the receptive field.
C. The monkey makes a saccade that brings the position of the recent light flash into the receptive field.
A neuron in the lateral intraparietal area fires before a saccade to a stable object.
On each trial one object in a stable array becomes significant to the monkey because the monkey must make a saccade to it. The monkey fixates a point outside the array, and a cue that matches an object in the array appears outside the neuron's receptive field. The monkey must then make a saccade to the center of the array and a second saccade to the object that matches the cue. Two experiments are shown, each in three panels. The left panel shows the response to the cue when it appears outside the receptive field, the center panel shows the response after the first saccade that brings the cued object into the receptive field, and the right panel shows the response just before the saccade to the cued object. The cues are shown here in green for clarity but were black in the experiment.
A. The monkey is trained to make the second saccade to the cued object; the cell fires intensely when the first saccade brings the object into the receptive field.
B. The monkey is trained to make the second saccade to an object outside the receptive field; the cell fires much less when the saccade brings the task-irrelevant stimulus into the receptive field. The visual scene at the time of the saccade is identical in both experiments.
Neurons in the lateral intraparietal area collectively represent the entire visual hemifield, but the neurons active at any one moment represent only the important or salient objects in the hemifield. That is, a few salient objects—such as the goal of an eye movement or a recent flash—evoke responses in a subset of neurons, and the activity of these neurons is greater than the background activity of the entire population of cells. Both the attention mechanisms and saccades are directed to the peak of the map.
The absolute value of the response evoked by a salient stimulus does not determine whether the stimulus is the most likely saccade target or most highly attended stimulus. When a monkey plans a saccade to a stimulus in the visual field, attention is on the goal of the saccade, and the activity evoked by the saccade plan lies at the peak of the salience map. However, if a bright light appears elsewhere in the visual field, attention is involuntarily drawn to the bright light, which evokes more neuronal activity than does the saccade plan. Thus the locus of attention can be ascertained only by examining the entire salience map and choosing its peak; it cannot be identified by monitoring activity at one point alone.