Neurons in the Primate Superior Colliculus Coding for Arm Movements in Gaze-Related Coordinates

2000 ◽  
Vol 83 (3) ◽  
pp. 1283-1299 ◽  
Author(s):  
Veit Stuphorn ◽  
Erhard Bauswein ◽  
Klaus-Peter Hoffmann

In the intermediate and deep layers of the superior colliculus (SC), a well-established oculomotor structure, a substantial population of cells is involved in the control of arm movements. To examine the reference frame of these neurons, we recorded in two rhesus monkeys ( Macaca mulatta) the discharges of 331 neurons in the SC and the underlying mesencephalic reticular formation (MRF) while monkeys reached to the same target location during different gaze orientations. For 65 reach-related cells with sufficient data and for simultaneously recorded electromyograms (EMGs) of 11 arm muscles, we calculated an ANOVA (factors: target position, gaze angle) and a gaze-dependency (GD) index. EMGs and the activity of many (60%) of the reach-related neurons were not influenced by the target representation on the retina or eye position. We refer to these as “gaze-independent” reach neurons. For 40%, however, the GD fell outside the range of the muscle modulation, and the ANOVA showed a significant influence of gaze. These “gaze-related” reach neurons discharge only when the monkey reaches for targets having specific coordinates in relation to the gaze axis, i.e., for targets in a gaze-related “reach movement field” (RMF). Neuronal activity was not modulated by the specific path of the arm movement, the muscle pattern that is necessary for its realization or the arm that was used for the reach. In each SC we found gaze-related neurons with RMFs both in the contralateral and in the ipsilateral hemifield. The topographical organization of the gaze-related reach neurons in the SC could not be matched with the well-known visual and oculomotor maps. Gaze-related neurons were more modulated in their strength of activity with different directions of arm movements than were gaze-independent reach neurons. Gaze-related reach neurons were recorded at a median depth of 2.03 mm below SC surface in the intermediate layers, where they overlap with saccade-related burst neurons (median depth: 1.55 mm). Most of the gaze-independent reach cells were found in a median depth of 4.01 mm below the SC surface in the deep layers and in the underlying MRF. The gaze-related reach neurons operating in a gaze-centered coordinate system could signal either the desired target position with respect to gaze direction or the motor error between gaze axis and reach target. The gaze-independent reach neurons, possibly operating in a shoulder- or arm-centered reference frame, might carry signals closer to motor output. Together these two types of reach neurons add evidence to our hypothesis that the SC is involved in the sensorimotor transformation for eye-hand coordination in primates.

2003 ◽  
Vol 89 (3) ◽  
pp. 1456-1466 ◽  
Author(s):  
Hansjörg Scherberger ◽  
Melvyn A. Goodale ◽  
Richard A. Andersen

The selection of one of two visual stimuli as a target for a motor action may depend on external as well as internal variables. We examined whether the preference to select a leftward or rightward target depends on the action that is performed (eye or arm movement) and to what extent the choice is influenced by the target location. Two targets were presented at the same distance to the left and right of a fixation position and the stimulus onset asynchrony (SOA) was adjusted until both targets were selected equally often. This balanced SOA time is then a quantitative measure of selection preference. In two macaque monkeys tested, we found the balanced SOA shifted to the left side for left-arm movements and to the right side for right-arm movements. Target selection strongly depended on the horizontal target location. By varying eye, head, and trunk position, we found this dependency embedded in a head-centered behavioral reference frame for saccade targets and, somewhat counter-intuitively, for reach targets as well. Target selection for reach movements was influenced by the eye position, while saccade target selection was unaffected by the arm position. These findings suggest that the neural processes underlying target selection for a reaching movement are to a large extent independent of the coordinate frame ultimately used to make the limb movement, but are instead closely linked to the coordinate frame used to plan a saccade to that target. This similarity may be indicative of a common spatial framework for hand-eye coordination.


2004 ◽  
Vol 91 (4) ◽  
pp. 1608-1619 ◽  
Author(s):  
Robert L. White ◽  
Lawrence H. Snyder

Neurons in many cortical areas involved in visuospatial processing represent remembered spatial information in retinotopic coordinates. During a gaze shift, the retinotopic representation of a target location that is fixed in the world (world-fixed reference frame) must be updated, whereas the representation of a target fixed relative to the center of gaze (gaze-fixed) must remain constant. To investigate how such computations might be performed, we trained a 3-layer recurrent neural network to store and update a spatial location based on a gaze perturbation signal, and to do so flexibly based on a contextual cue. The network produced an accurate readout of target position when cued to either reference frame, but was less precise when updating was performed. This output mimics the pattern of behavior seen in animals performing a similar task. We tested whether updating would preferentially use gaze position or gaze velocity signals, and found that the network strongly preferred velocity for updating world-fixed targets. Furthermore, we found that gaze position gain fields were not present when velocity signals were available for updating. These results have implications for how updating is performed in the brain.


2010 ◽  
Vol 103 (6) ◽  
pp. 3153-3166 ◽  
Author(s):  
Vicente Reyes-Puerta ◽  
Roland Philipp ◽  
Werner Lindner ◽  
Klaus-Peter Hoffmann

When reaching for an object, primates usually look at their target before touching it with the hand. This gaze movement prior to the arm movement allows target fixation, which is usually prolonged until the target is reached. In this manner, a stable image of the object is provided on the fovea during the reach, which is crucial for guiding the final part of the hand trajectory by visual feedback. Here we investigated a neural substrate possibly responsible for this behavior. In particular we tested the influence of reaching movements on neurons recorded at the rostral pole of the superior colliculus (rSC), an area classically related to fixation. Most rSC neurons showed a significant increase in their activity during reaching. Moreover, this increase was particularly high when the reaching movements were preceded by corresponding saccades to the targets to be reached, probably revealing a stronger coupling of the oculo-manual neural system during such a natural task. However, none of the parameters tested—including movement kinematics and target location—was found to be closely related to the observed increase in neural activity. Thus the increase in activity during reaching was found to be rather nonspecific except for its dependence on whether the reach was produced in isolation or in combination with a gaze movement. These results identify the rSC as a neural substrate sufficient for gaze anchoring during natural reaching movements, placing its activity at the core of the neural system dedicated to eye-hand coordination.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Mohammad R. Saeedpour-Parizi ◽  
Shirin E. Hassan ◽  
Ariful Azad ◽  
Kelly J. Baute ◽  
Tayebeh Baniasadi ◽  
...  

AbstractThis study examined how people choose their path to a target, and the visual information they use for path planning. Participants avoided stepping outside an avoidance margin between a stationary obstacle and the edge of a walkway as they walked to a bookcase and picked up a target from different locations on a shelf. We provided an integrated explanation for path selection by combining avoidance margin, deviation angle, and distance to the obstacle. We found that the combination of right and left avoidance margins accounted for 26%, deviation angle accounted for 39%, and distance to the obstacle accounted for 35% of the variability in decisions about the direction taken to circumvent an obstacle on the way to a target. Gaze analysis findings showed that participants directed their gaze to minimize the uncertainty involved in successful task performance and that gaze sequence changed with obstacle location. In some cases, participants chose to circumvent the obstacle on a side for which the gaze time was shorter, and the path was longer than for the opposite side. Our results of a path selection judgment test showed that the threshold for participants abandoning their preferred side for circumventing the obstacle was a target location of 15 cm to the left of the bookcase shelf center.


1990 ◽  
Vol 4 (3) ◽  
pp. 289-298 ◽  
Author(s):  
James T. McIlwain

AbstractSaccades evoked electrically from the deep layers of the superior colliculus have been examined in the alert cat with its head fixed. Amplitudes of the vertical and horizontal components varied linearly with the starting position of the eye. The slopes of the linear-regression lines provided an estimate of the sensitivity of these components to initial eye position. In observations on 29 sites in nine cats, the vertical and horizontal components of saccades evoked from a given site were rarely influenced to the same degree by initial eye position. For most sites, the horizontal component was more sensitive than the vertical component. Sensitivities of vertical and horizontal components were lowest near the representations of the horizontal and vertical meridians, respectively, of the collicular retinotopic map, but otherwise exhibited no systematic retinotopic dependence. Estimates of component amplitudes for saccades evoked from the center of the oculomotor range also diverged significantly from those predicted from the retinotopic map. The results of this and previous studies indicate that electrical stimulation of the cat's superior colliculus cannot yield a unique oculomotor map or one that is in register everywhere with the sensory retinotopic map. Several features of these observations suggest that electrical stimulation of the colliculus produces faulty activation of a saccadic control system that computes target position with respect to the head and that small and large saccades are controlled differently.


2002 ◽  
Vol 87 (6) ◽  
pp. 2778-2789 ◽  
Author(s):  
Robijanto Soetedjo ◽  
Chris R. S. Kaneko ◽  
Albert F. Fuchs

Saccadic eye movements of different sizes and directions are represented in an orderly topographic map across the intermediate and deep layers of the superior colliculus (SC), where large saccades are encoded caudally and small saccades rostrally. Based on experiments in the cat, it has been suggested that saccades are initiated by a hill of activity at the caudal site appropriate for a particular saccade. As the saccade evolves and the remaining distance to the target, the motor error, decreases, the hill moves rostrally across successive SC sites responsible for saccades of increasingly smaller amplitudes. When the hill reaches the “fixation zone” in the rostral SC, the saccade is terminated. A moving hill of activity has also been posited for the monkey, in which it is supposed to be transported via so-called build-up neurons (BUNs), which have a prelude of activity that culminates in a burst for saccades. However, several studies using a variety of approaches have yet to provide conclusive evidence for or against a moving hill. The moving hill scenario predicts that during a large saccade the burst of a BUN in the rostral SC will be delayed until the motor error remaining in the evolving saccade is equal to the saccadic amplitude for which that BUN discharges best, i.e., its optimal amplitude. Therefore a plot of the burst lead preceding the “optimal” motor error against the time of occurrence of the optimal motor error should have a slope of zero. A slope of −1 indicates no moving hill. For our 20 BUNs, we used three measures of burst timing: the leads to the onset, peak, and center of the burst. The average slopes of these relations were −1.09, −0.79, and −0.58, respectively. For individual BUNs, the slopes of all three relations always differed significantly from zero. Although the peak and center leads fall between −1 and 0, a hill of activity moving rostrally at a rate indicated by either of these slopes would arrive at the fixation zone much too late to terminate the saccade at the appropriate time. Calculating our same three timing measures from averaged data leads us to the same conclusion. Thus our data do not support the moving hill model. However, we argue in the discussion that the constant lead of the burst onset relative to saccade onset (∼27 ms) suggests that the BUNs may help to trigger the saccade.


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