Effect of Short-Term Saccadic Adaptation on Saccades Evoked by Electrical Stimulation in the Primate Superior Colliculus

2002 ◽  
Vol 87 (4) ◽  
pp. 1915-1923 ◽  
Author(s):  
Jay A. Edelman ◽  
Michael E. Goldberg

The brain maintains the accuracy of visually guided movements by using visual feedback to correct for changes in the nervous system and musculature that would otherwise result in dysmetria. In monkeys, evidence suggests that an adaptive mechanism can compensate for weakness in an extraocular muscle by changing the gain of the neural signal to the weakened muscle. The visual effects of such neuromuscular changes have been simulated using a short-term saccade adaptation paradigm, in which the target spot jumps to a new location during the initial saccade. Under these circumstances, over several hundred trials, monkeys gradually change the amplitude of their saccades so that the eye lands closer to the final location of the target spot. There is considerable evidence from lesion and single-unit recording studies that the locus of such saccade adaptation is downstream of the superior colliculus in the cerebellum. Paradoxically, previous research has indicated that saccades evoked by electrical stimulation in the superior colliculus are not modified by short-term saccade adaptation, suggesting that adaptation occurs in the oculomotor system upstream of the superior colliculus or else in a pathway that bypasses the superior colliculus. We tested whether this result was due to using suprathreshold stimulation currents. Stimulating at 44 low-threshold sites in the superior colliculi of three monkeys revealed that using low current levels evoked saccades that were modified by adaptation. Adaptation for visually guided and electrically evoked saccades had similar time courses and tended to be accomplished by a reduction in saccade velocity rather than a decrease in duration. Moreover, the more similar the velocity of electrically evoked and visually guided saccades prior to the start of saccadic adaptation the greater the effect of adaptation on electrically evoked saccades. These results suggest that the superior colliculus is indeed upstream of the locus of adaptation, corroborating previous lesion and single-cell recording studies, but that the mechanism mediating saccade adaptation is sensitive to the parameters of electrical stimulation.

2004 ◽  
Vol 92 (4) ◽  
pp. 2261-2273 ◽  
Author(s):  
Yoshiko Izawa ◽  
Hisao Suzuki ◽  
Yoshikazu Shinoda

To understand the neural mechanism of fixation, we investigated effects of electrical stimulation of the frontal eye field (FEF) and its vicinity on visually guided (Vsacs) and memory-guided saccades (Msacs) in trained monkeys and found that there were two types of suppression induced by the electrical stimulation: suppression of ipsilateral saccades and suppression of bilateral saccades. In this report, we characterized the properties of the suppression of bilateral Vsacs and Msacs. Stimulation of the bilateral suppression sites suppressed the initiation of both Vsacs and Msacs in all directions during and ∼50 ms after stimulation but did not affect the vector of these saccades. The suppression was stronger for ipsiversive larger saccades and contraversive smaller saccades, and saccades with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for the suppression of ipsilateral and contralateral Vsacs was ∼40–50 ms before saccade onset, indicating that the suppression occurred most likely in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of bilateral saccades were located in the prearcuate gyrus facing the inferior arcuate sulcus where stimulation induced suppression at ≤40 μA but usually did not evoke any saccades at 80 μA and were different from those of ipsilateral saccades where stimulation evoked saccades at ≤50 μA. The bilateral suppression sites contained fixation neurons. The results suggest that fixation neurons in the bilateral suppression area of the FEF may play roles in maintaining fixation by suppressing saccades in all directions.


2008 ◽  
Vol 100 (2) ◽  
pp. 1098-1112 ◽  
Author(s):  
Ping Liu ◽  
Michele A. Basso

The inhibitory drive arising from the basal ganglia is thought to prevent the occurrence of orienting movements of the eyes, head, and body in monkeys and other mammals. The direct projection from the substantia nigra pars reticulata (SNr) to the superior colliculus (SC) mediates the inhibition. Since the original experiments in the SNr of monkeys the buildup or prelude neuron has been a focus of SC research. However, whether the SNr influences buildup neurons in SC is unknown. Furthermore, a contralateral SNr–SC pathway is evident in many species but remains unexplored in the alert monkey. Here we introduced electrical stimulation of one or both SNr nuclei while recording from SC buildup neurons. Stimulation of the SNr reduced the discharge rate of SC buildup neurons bilaterally. This result is consistent with activation of an inhibitory drive from SNr to SC. The time course of the influence of ipsilateral SNr on the activity of most SC neurons was longer (∼73 ms) than the influence of the contralateral SNr (∼34 ms). We also found that the variability of saccade onset time and saccade direction was altered with electrical stimulation of the SNr. Taken together our results show that electrical stimulation activates the inhibitory output of the SNr that in turn, reduces the activity of SC buildup neurons in both hemispheres. However, rather than acting as a gate for saccade initiation, the results suggest that the influence of SNr inhibition on visually guided saccades is more subtle, shaping the balance of excitation and inhibition across the SC.


1992 ◽  
Vol 67 (4) ◽  
pp. 1000-1002 ◽  
Author(s):  
D. P. Munoz ◽  
R. H. Wurtz

1. In the rostral pole of the monkey superior colliculus (SC) a subset of neurons (fixation cells) discharge tonically when a monkey actively fixates a target spot and pause during the execution of saccadic eye movements. 2. To test whether these fixation cells are necessary for the control of visual fixation and saccade suppression, we artificially inhibited them with a local injection of muscimol, an agonist of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA). After injection of muscimol into the rostral pole of one SC, the monkey was less able to suppress the initiation of saccades. Many unwanted visually guided saccades were initiated less than 100 ms after onset of a peripheral visual stimulus and therefore fell into the range of express saccades. 3. We propose that fixation cells in the rostral SC form part of a fixation system that facilitates active visual fixation and suppresses the initiation of unwanted saccadic eye movements. Express saccades can only occur when activity in this fixation system is reduced.


2012 ◽  
Vol 107 (12) ◽  
pp. 3342-3348 ◽  
Author(s):  
Thérèse Collins ◽  
Josh Wallman

When saccades systematically miss their visual target, their amplitude adjusts, causing the position errors to be progressively reduced. Conventionally, this adaptation is viewed as driven by retinal error (the distance between primary saccade endpoint and visual target). Recent work suggests that the oculomotor system is informed about where the eye lands; thus not all “retinal error” is unexpected. The present study compared two error signals that may drive saccade adaptation: retinal error and prediction error (the difference between predicted and actual postsaccadic images). Subjects made saccades to a visual target in two successive sessions. In the first session, the target was extinguished during saccade execution if the amplitude was smaller (or, in other experiments, greater) than the running median, thereby modifying the average retinal error subjects experienced without moving the target during the saccade as in conventional adaptation paradigms. In the second session, targets were extinguished at the start of saccades and turned back on at a position that reproduced the trial-by-trial retinal error recorded in the first session. Despite the retinal error in the first and second sessions having been identical, adaptation was severalfold greater in the second session, when the predicted target position had been changed. These results argue that the eye knows where it lands and where it expects the target to be, and that deviations from this prediction drive saccade adaptation more strongly than retinal error alone.


1996 ◽  
Vol 13 (2) ◽  
pp. 237-246 ◽  
Author(s):  
Yi Zhang ◽  
Richard D. ◽  
Carol A. Bennett-Clarke ◽  
Robert W. Rhoades

AbstractAutoradiography with 125I-neurotensin in normal and enucleated hamsters was used to define the distribution of receptors for this peptide in the superficial layers of the superior colliculus (SC). Neurotensin binding sites were densely distributed in the stratum griseum superficiale (SGS), and results from the enucleated animals indicated that they were not located on retinal axons. The effects of neurotensin on individual superficial layer cells were tested in single-unit recording experiments. Neurotensin was delivered via micropressure ejection during visual stimulation (n = 75 cells), or during electrical stimulation of either the optic chiasm (OX; n = 47 cells) or visual cortex (CTX; n = 29 cells). In comparison with control values, application of neurotensin decreased visual responses of all SC cells tested to 54.1 ± 34.9% (mean ± standard deviation; range of decrement 7.5 to 100%; nine cells showed no effect or an increase in visual activity, which for four of these was ≥30%). Neurotensin application also reduced responses to electrical stimulation of either OX or CTX, respectively, to 65.8 ± 36.5% of control values (range of decrement 2.6 to 97.4%; 12 neurons showed a weak increment ≤ 30%) and 68.0 ± 38.5% (range of decrement 3.3 to 100%; five cells showed no effect or an increment, in one case ≥ 30%). Of the 25 neurons tested with both OX and CTX stimulation, the correlation of evoked response suppression by neurotensin was highly significant (r = 0.70; P < 0.001). This suggests that the suppressive effects of neurotensin were common to both pathways. To test whether the inhibitory effects of neurotensin were presynaptic or postsynaptic, Mg2+ ions were ejected iontophoretically to abolish synaptic responses, and the neurons (n = 16) were activated by iontophoresis of glutamate and then tested with neurotensin. Neurotensin reduced the glutamate-evoked responses to an average 59.3 ± 37.9% of control values (range 2.3 to 92.5%; one cell showed an increment >30%). This result suggests that the site of action of neurotensin is most likely postsynaptic.


2021 ◽  
pp. 1-10
Author(s):  
Michihiro Osumi ◽  
Daisuke Shimizu ◽  
Yuki Nishi ◽  
Shu Morioka

Background: Patients with brachial plexus avulsion (BPA) usually experience phantom sensations and phantom limb pain (PLP) in the deafferented limb. It has been suggested that evoking the sensation of touch in the deafferented limb by stimulating referred sensation areas (RSAs) on the cheek or shoulder might alleviate PLP. However, feasible rehabilitation techniques using this approach have not been reported. Objective: The present study sought to examine the analgesic effects of simple electrical stimulation of RSAs in BPA patients with PLP. Methods: Study 1: Electrical stimulation of RSAs for 60 minutes was conducted for six BPA patients suffering from PLP to examine short-term analgesic effects. Study 2: A single case design experiment was conducted with two BPA patients to investigate whether electrical stimulation of RSAs was more effective for alleviating PLP than control electrical stimulation (electrical stimulation of sites on side opposite to the RSAs), and to elucidate the long-term effects of electrical stimulation of RSAs. Results: Study 1: Electrical stimulation of RSAs evoked phantom touch sensations in the deafferented limb, and significantly alleviated PLP (p <  0.05). Study 2: PLP was alleviated more after electrical stimulation on RSAs compared with control electrical stimulation (p <  0.05). However, the analgesic effects of electrical stimulation on RSAs were observed only in the short term, not in the long term (p >  0.05). Conclusions: Electrical stimulation of RSAs not only evoked phantom touch sensation but also alleviated PLP in the short term. The results indicate that electrical stimulation of RSAs may provide a useful practical rehabilitation technique for PLP. Future studies will be required to clarify the mechanisms underlying immediate PLP alleviation via electrical stimulation of RSAs.


1993 ◽  
Vol 69 (3) ◽  
pp. 953-964 ◽  
Author(s):  
P. W. Glimcher ◽  
D. L. Sparks

1. The first experiment of this study determined the effects of low-frequency stimulation of the monkey superior colliculus on spontaneous saccades in the dark. Stimulation trains, subthreshold for eliciting short-latency fixed-vector saccades, were highly effective at biasing the metrics (direction and amplitude) of spontaneous movements. During low-frequency stimulation, the distribution of saccade metrics was biased toward the direction and amplitude of movements induced by suprathreshold stimulation of the same collicular location. 2. Low-frequency stimulation biased the distribution of saccade metrics but did not initiate movements. The distribution of intervals between stimulation onset and the onset of the next saccade did not differ significantly from the distribution of intervals between an arbitrary point in time and the onset of the next saccade under unstimulated conditions. 3. Results of our second experiment indicate that low-frequency stimulation also influenced the metrics of visually guided saccades. The magnitude of the stimulation-induced bias increased as stimulation current or frequency was increased. 4. The time course of these effects was analyzed by terminating stimulation immediately before, during, or after visually guided saccades. Stimulation trains terminated at the onset of a movement were as effective as stimulation trains that continued throughout the movement. No effects were observed if stimulation ended 40–60 ms before the movement began. 5. These results show that low-frequency collicular stimulation can influence the direction and amplitude of spontaneous or visually guided saccades without initiating a movement. These data are compatible with the hypothesis that the collicular activity responsible for specifying the horizontal and vertical amplitude of a saccade differs from the type of collicular activity that initiates a saccade.


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.


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