Neuromagnetic signatures of the spatiotemporal transformation for manual pointing.

Movement planning involves transforming the sensory signals into a command in motor coordinates. Surprisingly, the real-time dynamics of sensorimotor transformations at the whole brain level remain unknown, in part due to the spatiotemporal limitations of fMRI and neurophysiological recordings. Here, we used magnetoencephalography (MEG) during pro-/anti-wrist pointing to determine (1) the cortical areas involved in transforming visual signals into appropriate hand motor commands, and (2) how this transformation occurs in real time, both within and across the regions involved. We computed sensory, motor, and sensorimotor indices in 16 bilateral brain regions for direction coding based on hemispherically lateralized de/synchronization in the α (7-15 Hz) and ß (15-35 Hz) bands. We found a visuomotor progression, from pure sensory codes in 'early' occipital-parietal areas, to a temporal transition from sensory to motor coding in the majority of parietal-frontal sensorimotor areas, to a pure motor code, in both the α and ß bands. Further, the timing of these transformations revealed a top-down pro/anti cue influence that propagated 'backwards' from frontal through posterior cortical areas. These data directly demonstrate a progressive, real-time transformation both within and across the entire occipital-parietal-frontal network that follows specific rules of spatial distribution and temporal order.

Comparison of memory- and visually guided saccades using event-related fMRI.

Previous functional imaging studies have shown an increased hemodynamic signal in several cortical areas when subjects perform memory-guided saccades than that when they perform visually guided saccades using blocked trial designs. It is unknown, however, whether this difference results from sensory processes associated with stimulus presentation, from processes occurring during the delay period before saccade generation, or from an increased motor signal for memory-guided saccades. We conducted fMRI using an event-related paradigm that separated stimulus-related, delay-related, and saccade-related activity. Subjects initially fixated a central cross, whose color indicated whether the trial was a memory- or a visually guided trial. A peripheral stimulus was then flashed at one of 4 possible locations. On memory-guided trials, subjects had to remember this location for the subsequent saccade, whereas the stimulus was a distractor on visually guided trials. Fixation cross disappearance after a delay period was the signal either to generate a memory-guided saccade or to look at a visual stimulus that was flashed on visually guided trials. We found slightly greater stimulus-related activation for visually guided trials in 3 right prefrontal regions and right rostral intraparietal sulcus (IPS). Memory-guided trials evoked greater delay-related activity in right posterior inferior frontal gyrus, right medial frontal eye field, bilateral supplementary eye field, right rostral IPS, and right ventral IPS but not in middle frontal gyrus. Right precentral gyrus and right rostral IPS exhibited greater saccade-related activation on memory-guided trials. We conclude that activation differences revealed by previous blocked experiments have different sources in different areas and that cortical saccade regions exhibit delay-related activation differences.

Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements.

In humans, functional imaging studies have demonstrated a homologue of the macaque motion complex, MT+ [suggested to contain both middle temporal (MT) and medial superior temporal (MST)], in the ascending limb of the inferior temporal sulcus. In the macaque monkey, motion-sensitive areas MT and MST are adjacent in the superior temporal sulcus. Electrophysiological research has demonstrated that while MT receptive fields primarily encode the contralateral visual field, MST dorsal (MSTd) receptive fields extend well into the ipsilateral visual field. Additionally, macaque MST has been shown to receive extraretinal smooth-pursuit eye-movement signals, whereas MT does not. We used functional magnetic resonance imaging (fMRI) and the neural properties that had been observed in monkeys to distinguish putative human areas MT from MST. Optic flow stimuli placed in the full field, or contralateral field only, produced a large cluster of functional activation in our subjects consistent with previous reports of human area MT+. Ipsilateral optic flow stimuli limited to the peripheral retina produced activation only in an anterior subsection of the MT+ complex, likely corresponding to putative MSTd. During visual pursuit of a single target, a large portion of the MT+ complex was activated. However, during nonvisual pursuit, only the anterolateral portion of the MT+ complex was activated. This subsection of the MT+ cluster could correspond to putative MSTl (lateral). In summary, we observed three distinct subregions of the human MT+ complex that were arranged in a manner similar to that seen in the monkey.

A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing.

An anti-saccade, which is a saccade directed toward a mirror-symmetrical position in the opposite visual field relative to the visual stimulus, involves at least three separate operations: covert orienting, response suppression, and coordinate transformation. The distinction between pro- and anti-saccades can also be applied to pointing. We used fMRI to compare patterns of brain activation during pro- and anti-movements, to determine whether or not additional areas become active during the production of anti-movements. In parietal cortex, an inferior network was active during both saccades and pointing that included three foci along the intraparietal sulcus: 1) a posterior superior parietal area (pSPR), more active during the anti-tasks; 2) a middle inferior parietal area (mIPR), active only during the anti-tasks; and 3) an anterior inferior parietal area (aIPR), equally active for pro- and anti-movement. A superior parietal network was active during pointing but not saccades and included the following: 1) a medial region, active during anti- but not pro-pointing (mSPR); 2) an anterior and medial region, more active during pro-pointing (aSPR); and 3) an anterior and lateral region, equally active for pro- and anti-pointing (lSPR). In frontal cortex, areas selectively active during anti-movement were adjacent and anterior to areas that were active during both the anti- and pro-tasks, i.e., were anterior to the frontal eye field and the supplementary motor area. All saccade areas were also active during pointing. In contrast, foci in the dorsal premotor area, the anterior superior frontal region, and anterior cingulate were active during pointing but not saccades. In summary, pointing with central gaze activates a frontoparietal network that includes the saccade network. The operations required for the production of anti-movements recruited additional frontoparietal areas.

Eye position signal modulates a human parietal pointing region during memory-guided movements.

Using functional magnetic resonance imaging, we examined the signal in parietal regions that were selectively activated during delayed pointing to flashed visual targets and determined whether this signal was dependent on the fixation position of the eyes. Delayed pointing activated a bilateral parietal area in the intraparietal sulcus (rIPS), rostral/anterior to areas activated by saccades. During right-hand pointing to centrally located targets, the left rIPS region showed a significant increase in activation when the eye position was rightward compared with leftward. As expected, activation in motor cortex showed no modulation when only eye position changed. During pointing to retinotopically identical targets, the left rIPS region again showed a significant increased signal when the eye position was rightward compared with leftward. Conversely, when pointing with the left arm, the right rIPS showed an increase in signal when eye position was leftward compared with rightward. The results suggest that the human parietal hand/arm movement region (rIPS), like monkey parietal areas (Andersen et al., 1985), exhibits an eye position modulation of its activity; modulation that may be used to transform the coordinates of the retinotopically coded target position into a motor error command appropriate for the wrist.

Does a monocularly presented size-contrast illusion influence grip aperture?

The present study tested the idea that if subjects rely more on scene-based pictorial cues when binocular cues are not available, then both their perceptual judgements and their grasp might be influenced by pictorial illusions such as the Ebbinghaus (Titchener) Circles Illusion under monocular viewing conditions. Under binocular viewing conditions, subjects were always able to scale their grip accurately to the true size of the target disc and were unaffected by the illusion. Under monocular viewing, however, subjects appeared to be influenced by the illusion. Thus, when confronted with physically different target discs displayed on backgrounds that made them appear equivalent in size, subjects treated the two discs as equivalent--even when picking them up. These results, combined with earlier work from our laboratory suggests that binocular information plays a critical role in normal human prehension but when this information is not available the visuomotor system is able to "fall back" on the remaining monocular cues, which can cause the visuomotor system to be more susceptible to pictorial illusions.

Visual test of Listing's law during vergence.

A simple visual test was used to measure how much Listing's plane rotates as a function of the vergence angle. This test measured the elevation-dependent torsional disparity of horizontal and vertical lines during three tasks: vergence on a near target, vergence through prisms that remained fixed, and through prisms that rotated with eye elevation. Consistent with our previous search-coil measurements, the results here suggest that the angle between the Listing's planes of the two eyes is somewhat less than the vergence angle.

Using a synoptophore to test Listing's law during vergence in normal subjects and strabismic patients.

The synoptophore was used to measure torsional interocular disparity. This, in turn, was used to compute how much the angle between the Listing's plane (LP) of the two eyes changes as a function of the vergence angle. The ratio of these two angles was defined as G. We measured G in normals and in patients suffering from intermittent horizontal strabismus. Consistent with previous search-coil experiments and with our previous visual test measures, the results using the synoptophore suggest that, for normals, G is less than 1. In the patient group the mean G was similar in magnitude but more variable. The variations in G did not appear to be related to the patient's measurement of ocular deviation. This result suggests that the vergence-related rotation of LP in these patients may be related to other factors besides the effort required to fuse the lines of sight.

Task-dependent changes in the shape and thickness of Listing's plane.

We examined the 2D surface formed by 3D eye positions of normal subjects to determine whether the shape and thickness changed in tasks that differed in saccadic directions: random, horizontal, vertical, radial, clockwise and counter-clockwise. Eye positions during the random task did not lie precisely on Listing's plane but on a surface with a small twist. This twist was present before, during, and after saccades. The degree of twist changed with the task; becoming less twisted for horizontal tasks and more twisted in the vertical tasks. The surface thickness changed with the task becoming thicker for multidirectional tasks. This greater thickness may occur because surfaces obtained in multidirectional tasks are the composite of surfaces with slightly different shapes.

Size-contrast illusions deceive the eye but not the hand.

BACKGROUND: When we reach out to pick up an object, not only do we direct our moving limb towards the location of the object, but the opening between our fingers and thumb is scaled in flight to the object's size. Evidence obtained from patients with neurological disorders has shown that the visual processing underlying the calibration of grip aperture and other movement parameters during grasping is mediated by visual mechanisms located in the cerebral cortex that are quite distinct from those underlying the experiential perception of object size and other object features. Under appropriate conditions, such dissociations can also be observed in individuals with normal vision. Here we present evidence that the calibration of grasp is quite refractory to pictorial illusions that have large effects on perceptual judgements of size. RESULTS: We used a variation of the familiar 'Titchener circles' illusion in which two target circles of equal size, each surrounded by a circular array of either smaller or larger circles, are presented side by side. Subjects typically report that the target circle surrounded by the array of smaller circles appears to be larger than the target surrounded by larger circles. In our test, two thin 'pokerchip' discs were used as the target circles. The relative size of the two discs was randomly varied so that on some trials the discs appeared perceptually different but were physically equivalent in size, and on other trials they were physically different but appeared perceptually equivalent. The perceptual judgements made by the 14 subjects in our experiment were strongly affected by this size-contrast illusion. However, when asked to pick up a disc, the scaling of the subjects grip aperture (measured opto-electronically before contact with the disc) was largely determined by the true size of the target disc and not its illusory size. CONCLUSIONS: It would seem that the automatic and metrically accurate calibrations required for skilled actions are mediated by visual processes that are separate from those mediating our conscious experiential perception. Earlier studies on patients with neurological deficits suggest that these two types of processing may depend on quite separate, but interacting, visual pathways in the cerebral cortex.

Polypropylene pellets as an inexpensive reusable substitute for milk in the Morris milk maze.

A new inexpensive opaquing agent for the Morris milk maze is described. Small light-weight polypropylene pellets that float on the surface of the water were used to eliminate visual cues about the location of the hidden platform without impeding swimming or the use of distal spatial cues. Results obtained using the pellets are identical to those obtained with milk powder as an opaquing agent. An automatic tracking system works as well with the pellet as with the milk version of the maze.