The neural structure responsible for perceptual mislocalization at the time of saccades is not known. However, presumptive visual and oculomotor structures are known to undergo dynamic changes around the time of each saccade, and here, we consider two possible neural mechanisms that might underlie postsaccadic spatial expansion, one based on the visual cortex and the other on the superior colliculus.
First, in the visual cortex, the spatial structure of the receptive fields of neurons in the lateral intraparietal (LIP) area, which is functionally related to saccadic eye movements and spatial information processing, change immediately before a saccade (
Duhamel, Colby, & Goldberg, 1992;
Ben Hamed, Duhamel, Bremmer & Graf, 2002;
Kusunoki & Goldberg, 2003). Receptive fields in other areas of the extrastriate cortex have also been found to be dynamic. Some neurons in these areas have receptive fields that expand at the time of saccades, becoming responsive to stimuli in both the old and new receptive fields (
Nakamura & Colby, 2002). On the other hand, some neurons in area V4 have receptive fields that become smaller before saccade onset (
Tolias, Moore, Smirnakis, Tehovnik, Siapas & Schiller, 2001). Although it is not clear how these changes in the spatial structure of the receptive fields relate to spatial mislocalization in most cases, there is evidence that the positional information decoded from neural activities of the medial temporal and medial superior temporal areas reflects the spatial mislocalization at the time of saccades (
Krekelberg, Kubischik, Hoffmann, & Bremmer, 2003). Considering the dynamic nature of receptive fields in the visual system revealed by previous studies, we can postulate that immediately after the termination of an eye movement, the receptive fields of individual neurons in the cortical areas specialized for visuospatial information processing might change temporarily for recalibration of spatial information. This would be a counterpart mechanism of the presaccadic change in receptive fields.
Next, we consider a hypothetical mechanism involving the superior colliculus that could underlie the two-dimensional spatial mislocalization found in the current study. Execution of a saccade and spatial processing of a visual target both involve neural activations within topographic map. The SC is related to spatial orientation involving the eye, head, pinna, and body movements (
Sparks & Hartwich-Young, 1989). Its neurons show both visual responses and saccade-related discharges. Furthermore, the SC undergoes a transient change immediately after execution of a saccade as described by
Nichols & Sparks (1995) and
Schlag, Pouget, Sadeghpour, & Schlag-Rey (1998). In their experiments, immediately after a visually-guided saccade a second saccade is evoked with electrical stimulation of the SC. The amplitude and direction of a saccade evoked by an electrical stimulation of the SC depended on the amplitude and direction of the preceding visually-guided saccade, and the direction of the electrically-evoked saccade was in the direction away from the preceding visually-guided saccade.
Suppose the subject first makes a 12 deg saccade to the right. This will result in an activation of a neural population within the topographic map of the SC. A simultaneous electrical stimulation of two separate sites within the SC evokes a vector-averaged saccade (
Robinson, 1972). Furthermore, two simultaneously-presented visual targets are localized between the two. In other words, one activation within a topographic map draws the other toward its location, probably because of a population average process. What will happen if one activation within a topographic map precedes the other? We propose that two sequential activation interacts differently within a topographic map due to a presumptive inhibitory phase following the initial excitation. The time course of the inhibitory phase ought be shorter than the refractory period of saccades, some 200ms. Thus, the initial activation due to execution of a 12 deg saccade undergoes temporary inhibition when another activation develops in other part of the map due to presentation of the LT (
Figure 14A). The LT produces neural activation within a circumscribed region in the SC, described as the ‘point-image’ by
Capuano & McIlwain (1981). The inhibitory influence from the preceding saccade on this population activity would modify the population average process as described by
Lee, Rohrer & Sparks (1988). In fact, the pattern of the saccade-induced error in localization of the LT is remarkably similar to the expanding pattern of saccadic dysmetria following a focal inactivation of the SC with direct injection of local anesthetic as described by
Lee, Rohrer & Sparks (1988). Whereas an excitatory activation will pull other simultaneous excitations toward itself, an inhibitory locus will push away other excitatory activations during localization, as the vector average process predicts (
Figure 14B). This interaction will produce mislocalization which is similar to the pattern of the saccade-induced error found in the current study. Some further unknown process might influence this neural interaction to account for the pattern of modulation by target location observed in the current study. Whether the active population of the SC during execution of a saccade undergoes an inhibitory phase immediately after a saccade remains to be seen.
The hypothetical process depicted in
Figure 14 need not be in the superior colliculus. Any topographic representation processing spatial information could be the candidate, and the critical element of the process is the interaction between the neural activations due to saccade execution and the appearance of a visual target within a topographic representation.
Morrone, Ross, & Burr (
1997) reported a spatial compression towards the saccade goal. In their experiment, the localization targets were briefly presented before a saccade was made toward another target presented earlier. The origin of compression appears to be the saccade goal, and thus their observations can also be interpreted as the result of neural interactions within a topographic map of a saccade target and a visual target presented before saccade start. Compression towards the fixation point observed by
Sheth & Shimojo (2001) also suggests an interaction within a topographic map. The neural activation related to fixation may interact with the activation due to the visual target, resulting in a compressing pattern.