Neuroscience Forefront ReviewSpatial updating and the maintenance of visual constancy
Section snippets
Definition
The term updating refers to the re-examination of a set of conditions after an event or a number of events have taken place. So, if a system has a known set of conditions at time 1, and one wishes to know the set of conditions of this same system at some later time (1+n), then one requires two pieces of information in order to update correctly: (1) the initial set of conditions of the system at time 1, and (2) information about any intervening event(s) that took place in the interim.
A familiar,
Spatial updating for saccadic eye movements
The first studies on spatial updating were conducted by Hallett and Lightstone 1976a, Hallett and Lightstone 1976b in which they designed the now classic double-step saccade task (Fig. 2). Here, subjects fixate a central target while two peripheral targets are briefly flashed in sequence (T1 followed by T2). The subject's task is to first make a saccade to the first target (T1) and then make a second saccade to the second target (T2). As in the target localization example above, the saccade to
The neural basis of spatial updating for saccadic eye movements
The neural substrate for spatial updating was first identified by a single-unit recording study examining this phenomenon in the lateral intraparietal area (LIP) of the posterior parietal cortex (Duhamel et al., 1992a; reviewed in Colby et al., 1995). Here, the receptive field of each neuron was first identified by illuminating visual stimuli at various spatial locations. The cell would respond whenever the stimulus was turned on in this particular spatial location (Fig. 3A). In a subsequent
Spatial updating during pursuit eye movements
Spatial updating has also been investigated for intervening pursuit eye movements. In these paradigms, subjects are asked to pursue a moving target until a second target is briefly flashed in the periphery. The subject's task is to make a saccade to the remembered, space-fixed location of the flashed target. But note that for a short period of time after the flash, the subject's eyes continue to pursue the moving target, even though it is no longer present. The subject can either make an
Are efference copies the source of the extra-retinal signal for spatial updating?
For saccades and pursuit, the source of the extra-retinal spatial updating signal is likely a motor efference copy [also known as corollary discharge (Sperry 1950, Von Holst and Mittlesteadt 1950)]. These signals are copies of voluntary, outgoing motor commands that are generated whenever we make a movement. For example, in order to move one's eyes, one must generate a neural command that is transmitted down to motoneurons in the brainstem that control the eye muscles. One can simply take a
Updating for self-motion
While versatile efference copies may work as an updating signal for eye movements made with the head and body fixed in space (e.g. saccades and pursuit), our everyday movements typically also involve movements of the head and body. For such movements, the vestibular system, which measures the body's inertial motion, is likely also involved. Specifically, three semicircular canals measure how the body rotates in three-dimensional space (i.e. yaw, pitch and roll), and two otolith organs (the
Pathways
Although all possible sensory and motor sources of updating signals have not yet been examined, it is becoming obvious that many originate in the brainstem, like vestibular signals and efference copies from the SC and oculomotor burst neurons. But evidence for neurons that perform spatial updating lies mainly in cortical areas including LIP (Duhamel et al 1992a, Kusunoki and Goldberg 2003, Heiser and Colby 2006), FEF (Goldberg and Bruce 1990, Umeno and Goldberg 1997, Umeno and Goldberg 2001)
Theoretical models of spatial updating
The mathematical computations that underlie spatial updating have also been described. As can be observed in Fig. 2, the correct updated ME to T2 in a double-step saccade task could theoretically be computed by subtracting the ME to T1 from the RE caused by T2 (i.e. green ME2=RE2−ME1). This formula is called vector subtraction and modeling it requires information pertaining to (1) the eye-centered representation of the visual target and (2) the metrics of the intervening movement.
Reference frames
Early behavioral evidence suggested that spatial constancy is partially maintained by a central representation of visual space in an allocentric (i.e. world-centered) reference frame (Dassonville et al 1995, Karn et al 1997; reviewed in Burgess, 2006). However, as summarized above, subsequent single unit recording experiments (e.g. Fig. 3), pointed toward a retinotopic (i.e. eye-centered) reference frame for spatial updating (Batista et al 1999, Kusunoki and Goldberg 2003, Heiser and Colby 2006
Conclusions
Spatial updating, the neural process underlying spatial constancy, is truly a complex and intriguing phenomenon. It combines RE signals with a variety of sensory and motor commands that describe the amplitude and direction of movements that occur between the time we see an object and when we decide to generate an action toward it. These intervening movements not only include eye movements such as saccades and pursuit, but also rotations of the head as well as whole-body rotations and
Acknowledgments
The authors would like to thank the following people for providing modified versions of their figures to this paper: Rebecca A. Berman, Gunnar Blohm, W. Pieter Medendorp and Min Wei. Support was provided by National Institutes of Health grant DC04260 to D.E.A.
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