Role of the Rostral Superior Colliculus in Gaze Anchoring During Reach Movements

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.

1999 ◽  
Vol 22 (4) ◽  
pp. 681-682 ◽  
Author(s):  
Michael C. Dorris ◽  
Douglas P. Munoz

The Findlay & Walker target article emphasizes the role of the target-nonspecific “fixate” system while downplaying the role of the target-specific “move” system in determining saccade latency. We agree that disengagement of the fixate system is responsible for the target-nonspecific latency reduction associated with the gap effect. However, high target predictability and extensive training at a target location can also result in latency reductions, the culmination of this being express saccades. The target-specificity associated with the latter forms of latency reduction implicate a mechanism involving the move system. Recently discovered neurophysiological correlates underlying these behavioural phenomena reside in the superior colliculus.


Author(s):  
Lars Lünenburger ◽  
Raimund Kleiser ◽  
Veit Stuphorn ◽  
Lee E. Miller ◽  
Klaus-Peter Hoffmann

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.


2001 ◽  
Vol 86 (2) ◽  
pp. 961-970 ◽  
Author(s):  
S.F.W. Neggers ◽  
H. Bekkering

A well-coordinated pattern of eye and hand movements can be observed during goal-directed arm movements. Typically, a saccadic eye movement precedes the arm movement, and its occurrence is temporally correlated with the start of the arm movement. Furthermore, the coupling of gaze and aiming movements is also observable after pointing initiation. It has recently been observed that saccades cannot be directed to new target stimuli, away from a pointing target stimulus. Saccades directed to targets presented during the final phase of a pointing movement were delayed until after pointing movement offset (“gaze anchoring”). The present study investigated whether ocular gaze is anchored to a pointing target during the entire pointing movement. In experiment 1, new targets were presented at various times during the duration of a pointing movement, triggered by the kinematics arm moment itself (movement onset, peak acceleration/velocity/deceleration, and offset). Subjects had to make a saccade to the new target as fast as possible while maintaining the pointing movement to the initial target. Saccadic latencies were increased by an amount of time that approximately equaled the remaining pointing time after saccadic target presentation, with the majority of saccades executed after pointing movement offset. The nature of the signal driving gaze stabilization during pointing was investigated in experiment 2. In previous experiments where ocular gaze was anchored to a pointing target, subjects could always see their moving arm, thus it was unknown whether a visual image of the moving arm, an afferent (proprioceptive) signal or an efferent (motor control related) signal produced gaze anchoring. In experiment 2 subjects had to point with or without vision of the moving arm to test whether a visual signal is used to anchor gaze to a pointing target. Results indicate that gaze anchoring was also observed without vision of the moving arm. The findings support the existence of a mechanism enforcing ocular gaze anchoring during the entire duration of a pointing movement. Moreover, such a mechanism uses an internally generated, or proprioceptive, nonvisual signal. Possible neural substrates underlying these processes are discussed, as well as the role of selective attention.


2018 ◽  
Vol 115 (16) ◽  
pp. E3817-E3826 ◽  
Author(s):  
Eric Mooshagian ◽  
Lawrence H. Snyder

We often orient to where we are about to reach. Spatial and temporal correlations in eye and arm movements may depend on the posterior parietal cortex (PPC). Spatial representations of saccade and reach goals preferentially activate cells in the lateral intraparietal area (LIP) and the parietal reach region (PRR), respectively. With unimanual reaches, eye and arm movement patterns are highly stereotyped. This makes it difficult to study the neural circuits involved in coordination. Here, we employ bimanual reaching to two different targets. Animals naturally make a saccade first to one target and then the other, resulting in different patterns of limb–gaze coordination on different trials. Remarkably, neither LIP nor PRR cells code which target the eyes will move to first. These results suggest that the parietal cortex plays at best only a permissive role in some aspects of eye–hand coordination and makes the role of LIP in saccade generation unclear.


2020 ◽  
Author(s):  
Preyaporn Phataraphruk ◽  
Qasim Rahman ◽  
Kishor Lakshminarayanan ◽  
Mitchell Fruchtman ◽  
Christopher A. Buneo

AbstractReaching movements are subject to noise arising during the sensing, planning and execution phases of movement production, which contributes to movement variability. When vision of the moving hand is available, reaching variability appears to be strongly influenced by noise occurring during the specification and/or online updating of movement plans in visual coordinates. In contrast, when vision of the hand is unavailable, variability appears more dependent upon hand movement direction, suggesting a greater influence of execution noise. Given that execution noise acts in part at the muscular level, we hypothesized that reaching variability should depend not only on movement direction but initial arm posture as well. Moreover, given that the effects of execution noise are more apparent when movements are performed without vision of the hand, we reasoned that postural effects would be more evident when visual feedback was withheld. To test these hypotheses, subjects planned memory-guided reaching movements to three frontal plane targets, using either an “adducted” or “abducted” initial arm posture. Movements were then executed with and without hand vision. We found that the effects of initial arm posture on movement variability were idiosyncratic in both visual feedback conditions. In addition, without visual feedback, posture-dependent differences in variability varied with movement extent, growing abruptly larger in magnitude during the terminal phases of movement, and were moderately correlated with differences in mean endpoint positions. The results emphasize the role of factors other than noise (i.e. biomechanics and suboptimal sensorimotor integration) in constraining patterns of movement variability in 3D space.


2005 ◽  
Vol 93 (1) ◽  
pp. 519-534 ◽  
Author(s):  
Masayuki Watanabe ◽  
Yasushi Kobayashi ◽  
Yuka Inoue ◽  
Tadashi Isa

To examine the role of competitive and cooperative neural interactions within the intermediate layer of superior colliculus (SC), we elevated the basal SC neuronal activity by locally injecting a cholinergic agonist nicotine and analyzed its effects on saccade performance. After microinjection, spontaneous saccades were directed toward the movement field of neurons at the injection site (affected area). For visually guided saccades, reaction times were decreased when targets were presented close to the affected area. However, when visual targets were presented remote from the affected area, reaction times were not increased regardless of the rostrocaudal level of the injection sites. The endpoints of visually guided saccades were biased toward the affected area when targets were presented close to the affected area. After this endpoint effect diminished, the trajectories of visually guided saccades remained modestly curved toward the affected area. Compared with the effects on endpoints, the effects on reaction times were more localized to the targets close to the affected area. These results are consistent with a model that saccades are triggered by the activities of neurons within a restricted region, and the endpoints and trajectories of the saccades are determined by the widespread population activity in the SC. However, because increased reaction times were not observed for saccades toward targets remote from the affected area, inhibitory interactions in the SC may not be strong enough to shape the spatial distribution of the low-frequency preparatory activities in the SC.


Author(s):  
Alison Pienciak-Siewert ◽  
Alaa A Ahmed

How does the brain coordinate concurrent adaptation of arm movements and standing posture? From previous studies, the postural control system can use information about previously adapted arm movement dynamics to plan appropriate postural control; however, it is unclear whether postural control can be adapted and controlled independently of arm control. The present study addresses that question. Subjects practiced planar reaching movements while standing and grasping the handle of a robotic arm, which generated a force field to create novel perturbations. Subjects were divided into two groups, for which perturbations were introduced in either an abrupt or gradual manner. All subjects adapted to the perturbations while reaching with their dominant (right) arm, then switched to reaching with their non-dominant (left) arm. Previous studies of seated reaching movements showed that abrupt perturbation introduction led to transfer of learning between arms, but gradual introduction did not. Interestingly, in this study neither group showed evidence of transferring adapted control of arm or posture between arms. These results suggest primarily that adapted postural control cannot be transferred independently of arm control in this task paradigm. In other words, whole-body postural movement planning related to a concurrent arm task is dependent on information about arm dynamics. Finally, we found that subjects were able to adapt to the gradual perturbation while experiencing very small errors, suggesting that both error size and consistency play a role in driving motor adaptation.


1997 ◽  
Vol 7 (4) ◽  
pp. 303-310
Author(s):  
James R. Lackner ◽  
Paul DiZio

The reafference model has frequently been used to explain spatial constancy during eye and head movements. We have found that its basic concepts also form part of the information processing necessary for the control and recalibration of reaching movements. Reaching was studied in a novel force environment–a rotating room that creates centripetal forces of the type that could someday substitute for gravity in space flight, and Coriolis forces which are side effects of rotation. We found that inertial, noncontacting Coriolis forces deviate the path and endpoint of reaching movements, a finding that shows the inadequacy of equilibrium position models of movement control. Repeated movements in the rotating room quickly lead to normal movement patterns and to a failure to perceive the perturbing forces. The first movements made after rotation stops, without Coriolis forces present, show mirror-image deviations and evoke perception of a perturbing force even though none is present. These patterns of sensorimotor control and adaptation can largely be explained on the basis of comparisons of efference copy, reafferent muscle spindle, and cutaneous mechanoreceptor signals. We also describe experiments on human iocomotion using an apparatus similar to that which Mittelstaedt used to study the optomotor response of the Eristalis fly. These results show that the reafference principle relates as well to the perception of the forces acting on and exerted by the body during voluntary locomotion.


1999 ◽  
Vol 82 (4) ◽  
pp. 2020-2023 ◽  
Author(s):  
Michael Pasternack ◽  
Mathias Boller ◽  
Belinda Pau ◽  
Matthias Schmidt

We have recently found that GABAC receptor subunit transcripts are expressed in the superficial layers of rat superior colliculus (SC). In the present study we used immunocytochemistry to demonstrate the presence of GABAC receptors in rat SC at protein level. We also investigated in acute rat brain slices the effect of GABAA and GABAC receptor agonists and antagonists on stimulus-evoked extracellular field potentials in SC. Electrical stimulation of the SC optic layer induced a biphasic, early and late, potential in the adjacent superficial layer. The late component was completely inhibited by 6-cyano-7-nitroquinoxaline-2,3-dione or CoCl2, indicating that it was generated by postsynaptic activation. Muscimol, a potent GABAA and GABAC receptor agonist, strongly attenuated this postsynaptic potential at concentrations >10 μM. In contrast, the GABAC receptor agonist cis-aminocrotonic acid, as well as muscimol at lower concentrations (0.1–1 μM) increased the postsynaptic potential. This increase was blocked by (1,2,5,6-tetrahydropyridine-4-yl)methylphosphinic acid, a novel competitive antagonist of GABAC receptors. Our findings demonstrate the presence of functional GABAC receptors in SC and suggest a disinhibitory role of these receptors in SC neuronal circuitry.


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