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before, during or after a saccade (Kleiser et al., 2004). They found saccadic suppression of activity in several cortical areas, including V5 and V4. V5 is part of the M-pathway, and V4, although an important part of the P-pathway, also receives significant input from the M-pathway. So reduced neural activity in V4 would be consistent with suppression of the M-pathway (Burr, 2005).
So, why suppress the M-pathway and not the P-pathway? The image during a saccade is moving very rapidly, and would probably primarily stimulate the M-pathway. It is therefore important to suppress its action to allow the creation of a stable image of the external world. The P-pathway is probably not stimulated very much by the moving image during the saccade, so there has been no selective pressure to develop a mechanism to suppress its activity.
What happens if you don’t have saccades?
Saccades seem to be intrinsic to our perception of the world, so what would happen if we didn’t have them? The chances of someone having such a deficit are extremely unlikely, but just such an observer was reported by Ian Gilchrist and John Findlay (Gilchrist et al., 1997). A. I. was a female psychology undergraduate at Durham University where, by chance, her unusual vision was discovered by Gilchrist and Findlay, who were members of the Psychology faculty. As a result of a congenital degeneration of optic muscles, A. I. has had no eye movements since birth. However, she has no problems with reading or with any other visual task. The process of reading potentially provides a good example of how visual processes and eye movements are co-ordinated to sample the available visual information. Text is scanned in the typical saccadic manner, the eyes alternating between short rapid movements and brief fixations, during which time the gaze is stable (Gilchrist et al., 1997). Most saccades are to the right of the page, as the position of fixation jumps along the line of text. These saccades are usually seven to nine characters long, and the fixations between saccades last between 200 and 250 ms. It is during each fixation that information is gathered from the text. At the end of each line, the reader makes a return saccade to the left that places the eyes at the beginning of the next line.
So, without eye movements, how does A. I. manage to read? The answer seems to be that she uses movements of the head to compensate for the absence of eye movements (Gilchrist et al., 1997). Her head movements during reading show the same pattern of rapid ‘saccadic’ movements interspersed with ‘fixations’ (Figure 10.4). The ‘saccadic’ head movements tend to shift fixation position by approximately six characters, and the fixations themselves have an approximate duration of 200 ms. In addition, A. I. makes a characteristic large return movement at the end of each line. Her ‘head-saccades’ are not restricted to reading, but appear to be used in all viewing situations. When she views a picture, she uses ‘saccadic’
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Figure 10:4: (See also colour plate section.) An example of A.I.’s head movements while viewing one of Yarbus’s pictures. A.I.’s head movements are characteristic of normal eye movement during viewing such a picture (reproduced with permission from Gilchrist
et al., 1997. Copyright (1997)
Nature).
head movements to scan the scene broken by periods of fixation, suggesting that her saccadic head movements are how she usually explores a visual scene. All the movements used to move gaze position seem to have been transferred from the non-functional eye muscles to her neck muscles. Instead of her eyes being constantly on the move, her whole head is moving constantly to shift her gaze and allow her to sample the visual world.
How to stabilise the visual world
So how to stabilise your perception of the visual world when your eyes are constantly moving? Suppression of the motion sensitive M-pathway is only part of the story. Even if we don’t perceive the movement of the visual scene produced by our saccades, we still have to cope with the change in the visual scene produced by our eyes moving from one fixation point to another and integrate these snapshots of the world into a coherent percept. The basis of this stabilisation of our visual perception seems to be based at least partially on monitoring eye movement commands. As mentioned earlier in this chapter, in parallel with the motor signal generating a saccade, a second copy is sent to the visual system to be used to compensate for the eye movement. This is called the corollary discharge.
The superior colliculus (SC), a multi-layered structure located at the top of the brainstem (Figure 10.5), plays an important role in the
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FEF
MDN
SC
generation of eye movements (Carpenter, 2000). The upper layers of the SC contain a map of the visual world. The deeper layers contain motor neurons, which if electrically stimulated produce eye movements that return the position of the eye to specific positions in the visual world. The SC also generates a corollary signal that is relayed to the frontal eye field or FEF (an area known to be involved in the planning of voluntary saccades), by neurons in the medio-dorsal nucleus (MDN) of the thalamus. This signal allows visual neurons in the FEF to spatially shift their receptive fields in anticipation of the change of visual scene produced by a saccade (Munoz, 2006). So the FEF neurons compensate for the saccade before it happens, and this helps stabilise perception. It is possible to interrupt this pathway using a microinjection of muscimol (a neurotransmitter blocker) into the MDN (Sommer & Wurtz, 2002). This prevents the corollary signal from reaching the FEF. This, in turn, blocks the normal anticipatory shift in the FEF receptive fields in response to a saccade (Sommer & Wurtz, 2006) and appears to impair the accuracy with which a monkey is able to integrate the spatial position of previous fixations to form a stable perception of the visual world (Sommer & Wurtz, 2002).
Figure 10:5: (See also colour plate section.) A lateral view of a monkey brain, which illustrates the pathway for corollary discharge to interact with visual perception. There is a pathway that runs from the superior colliculus (SC) in the midbrain to the medio-dorsal nucleus (MDN) of the thalamus and then on to the frontal eye field (FEF). This pathway is believed to carry the corollary discharge from the SC to the FEF (redrawn from Munoz, 2006).
Navigating through the world: go with the flow?
So far, we have discussed the motion produced by our own eye movements. An additional source of global motion is derived from our own movement through the world. This movement produces a sensation called optic flow. Like eye movements, optic flow produces visual changes that cover the entire visual field, whereas the movement of an object in the environment covers only a part of it. Optic flow has long been thought to play a role in our ability to navigate through the environment. Oncoming objects can provide cues as to where you are heading as their images seem to expand from a central point in the visual field (the focus of expansion or FoE) (Figure 10.6). The FoE indicates the target towards which you are heading. It can also provide cues about the relative position of objects in the environment as nearer objects will appear to move faster than more distant ones. Eye movements add another dimension of difficulty to
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Figure 10:6: Three simulations of optic flow patterns that result from forward movement of the observer. The simulation in the centre illustrates the symmetric pattern produced when the eyes and head are directed straight ahead and the observer is moving straight ahead. Each line indicates the direction a particular point in the environment would take (away from the FOE). The length of the line indicates the speed of the motion. There are longer lines in the periphery indicating the perception of faster motion. In the simulation on the right, the observer is looking straight ahead but is heading towards the left, and so the FOE is also on the left. In the simulation on the right of the figure, the observer is looking straight ahead but heading to the right, and so the FOE is on the right (reproduced with permission from Wurtz, 1998. Copyright (1998) Elsevier).
this calculation, because the FoE will not remain in a fixed position on the retina. As we have seen above, our eyes are constantly moving, drawn to some interesting scene, or object or person. Thus, to use optic flow to calculate the direction in which you are heading, your brain has to compensate for these movements.
For example, when observers sit facing an expanding image on a computer monitor, they experience the sensation of moving through space. However, if the observers are asked to move their eyes to track the movement of a marker across the screen, the observers can still identify the heading direction as signalled by the FoE on the screen (Warren & Hannon, 1988, 1990). Thus, although the FoE on the screen is shifted across their retina by eye movements, the brain is still able to compensate and calculate the correct heading. In a variant of this experiment, observers keep their eyes fixed on the same spot on the computer screen and the computer ‘shifts’ the screen image to simulate eye movements. This artificially alters the position of the expanding image and the FoE on the observer’s retina. As there are no eye movements, the brain has to rely on purely visual cues to compensate for the movement of image. Observers see themselves travelling on a false path that curves away from the actual heading (Royden, Banks & Crowell, 1992; Banks et al., 1996). This suggests that, under normal conditions, information from the corollary discharge allows the brain to compensate for eye movements and calculate heading from the remaining optic flow information.
The neural basis of this behaviour seems to be located in a subdivision of the medial superior temporal (MSTd) part of the parietal cortex. Single-cell recording from MSTd neurons, while monkeys watched flow fields on a computer screen, shows that each neuron fires most strongly when the FoE is in a particular part of the visual field and it reduces its firing rate as the FoE is shifted away from that area (Andersen, 1997). If the FOE is shifted in the visual field by the movement of the monkey’s eyes, nearly half the MSTd neurons tested seem to compensate for the shift and their firing rate remains unchanged. However, if the movement is produced by the computer and the eyes remain still, the neurons’ firing rate changes, suggesting that the neurons have problems compensating for the movement and maintaining an accurate representation of the true heading. It seems that the neurons need the corollary discharge signal to tell